parent report case study

CASE REPORT article

Case report: a case study significance of the reflective parenting for the child development.

• Department of Psychology, Plovdiv University “Paisii Hilendarski,” Plovdiv, Bulgaria

There are studies that connect the “child” in the past with the “parent” in the present through the prism of high levels of stress, guilt, anxiety. This raises the question of the experiences and internal work patterns formed in childhood and developed through parenthood at a later stage. The article (case study) presents the quality of parental capacity of a family raising a child with an autism spectrum. The abilities of parents (the emphasis is on the mother) to recognize and differentiate the mental states of their non-verbal child are discussed. An analysis of the parental representations for the child and the parent–child relationship is developed. The parameters of reflective parenting are measured. The methodology provides good opportunities for identifying deficits in two aspects: parenting and the functioning of the child itself. Without their establishment, therapy could not have a clear perspective. An integrative approach for psychological support of the child and his family is presented: psychological work with the child on the main areas of functioning, in parallel with the therapy conducted with the parents and the mother, as the main caregiver. The changes for the described period are indicated, which are related to the improvement of the parental capacity in the mother and the progress in the therapy in the child. A prognosis for ongoing therapy is given, as well as topics that have arisen in the process of diagnostic procedures.

Introduction

Attachment theory focuses on parent–child attachment and the effects this relationship has on the child's personality, interpersonal skills, and its capacity to form healthy relationships with adults. According to Bowlby (1969) , parents who are approachable and responsive allow their child to develop a sense of security, thus creating a sound basis for it to learn about the world. The capability of parents to verbalize the feelings and experiences of their child through conversations, reading stories or fairy tales, commenting on everyday situations develops the skills of mentalization in the child ( Ханчева, 2019 ).

In mature age, the ability to mentalize depends on the emotional load of the interpersonal situation. Optimal mentalization implies integration of cognitive knowledge with insights into the emotional world, which allows a man to see more clearly and achieve “emotional knowledge” ( Allen and Fonagy, 2006 ).

The processes of mentalization can be influenced by the “heritage” that is passed down through generations. In their life experience, individuals operate and make their choices not being aware that they repeat the history of their ancestors. In part, these complex relationships can be seen, felt, or anticipated. They are experienced as elusive, insensible, unnamed, or secret, and may leave traumatic traces ( Kellermann, 2001 ).

Tisseron (2011) , associates the process of transmission of traumatic experience from generation to generation with three types of symbolization of experience: affective/sensory/motor, figurative, and verbal. If the event is symbolized in just one of the modalities, the results are associated with violation of mental life. The result becomes a distortion of the parent–child relationships, of their functioning.

The main psychopathological mechanisms that are activated in the transmission of mental content between individuals from generation to generation are associated with the identification and the projective identity. In this case of transmission through generations, insensible patterns, conflicts, scenarios and roles, ideals, and perceptions of the object are identified.

Children of severely traumatic parents reproduce scenes that their parents went through, trying to understand their pain, and at the same time establish a connection with them. They maintain family ties through the integration of parenting experiences. In the meantime, the parent seeks to teach his/her child survival strategies in situations of future persecution, thus passing on his/her traumatic experience ( Baranowsky et al., 1998 ).

Wilgowicz (1999) , introduces the term “vampire complex” describing the impact of unexpressed and insensible experiences passed down from generation to generation. These traumatic experiences form the unconscious connection between the generations which interferes the natural course of the processes of separation and individuation. This complex is associated with experience of the child who in its development turns out to be “locked” in the prison of the parental traumatic experience being neither alive, nor dead, or in other words, unborn.

Krystal (1978) , describes the affective blindness of the principal caregiver as a characteristic of unprocessed traumatic experience ( Den Velde, 1998 ; Коростелева et al., 2017 ). It is associated with incomplete integration of the somatic Self into the Self.

Ammon (2000) , Hirsch (1994) describe in this context the “psychosomatic mother whose behavior is characterized by a lack of understanding of boundaries, intrusiveness, alexithymia, excessive concern for the physical functioning of her child, and at the same time “blind” to its psychic experiences.” Hope et al. (2019) report that maternal depression and complaints of psychological distress are associated with an increased risk of trauma and hospitalization for the age 3–11 years, with the highest being in the period 3–5 years. In another study, Baker et al. (2017) , reported an increased risk of burns, poisoning, and fractures in children aged 0–4 years raised by depressed mothers and/or such found in an anxious episode. Postpartum depression in the mother presupposes a high risk of burns, fractures, poisoning ( Nevriana et al., 2020 ).

The relationship between parental attitudes and child development is influenced by unconscious dynamics of the intrapsychic world of mother and father ( Tagareva, 2019 ). The ability of parents for reflexion and metacognitive monitoring allows them to recognize and regulate, to modulate, to turn into a symbolic (verbal) form the states they observe in their child. This gives an opportunity to comprehend and return in an understandable form to the child interpretation of its state based on understanding and empathy. If this capacity fails, the parent cannot give an adequate and meaningful interpretation of what is happening, because he/she himself/herself gets lost and confused in his/her own (threatening his/her integrity) experiences, and strong, meaningless, overwhelming emotions. The consequences of the lack of a “secure base” in the face of the caregiver may be associated with: low self-esteem, behavior of decompensation under stress, inability to develop and maintain friendships, trust and intimacy, pessimism toward themselves, family, society ( Matanova, 2015 ). The low level of reflexion on the trauma and the unaddressed traumatic experience as the mother's internal position, affect, and are a risk factor for, psychopathology later in the development.

In addition, parenting skills can be further tested when raising a child with Autism Spectrum Disorders in the family. Therapy for this nosology needs to include both psychological work with the child and support for the parents, especially for the mother, who in most cases limits her social roles and devotes herself only to parenthood. This is a serious argument to seek and optimize approaches in clinical practice to support the family environment in which children with neurodevelopmental disorders are raised.

Materials and Methods

This article is designed to present a case of a family with a child diagnosed with Autism Spectrum Disorder, where the non-integrated individual traumatic experience in the mother (N.) affects the quality of her reflective parenting.

The analysis aims to display the status of individual functioning and skills for reflective parenting, as well as the effectiveness of psychological intervention to revive and optimize the relationship mother-child. Although the functioning of the mother is the focus of the present study, an analysis of parenting and the father has also been applied.

The study is a pilot one and marks the start of a project lasting over time.

Diagnostic tools have been used for:

- Assessment of the development and functioning of the child according to the methodology of Matanova et al. ( Matanova and Todorova, 2013 ). The methodology includes research of cognitive, linguistic, social, emotional, and motor sphere of functioning. Based on the identified deficits, it is possible to arrange a therapeutic plan for the child.

- Self-assessment scales for the study of the quality of the parental relationship and the formed internal work patterns (of affection and romantic relationship) of N. with her parents:

° The Parental Reflective Functioning Questionnaire (PRFQ) by Luyten et al. (2017a , b ). The PRF assessment screening tool provides additional evidence of the complexity and multidimensionality of the PRF ( Luyten et al., 2009 ). It contains 18 items intended mainly for use in the study of PRF of parents with children aged 0–5 years. Three different aspects of PRF are evaluated on a 7-point Likert scale. Based on validated factor analysis, the authors identified three theoretically consistent and clinically significant factors, each of which included six items: (1) prementalization modes (PM), (2) certainty about mental states (CMS), (3) interest and curiosity about mental states (IC).

° Assessment of emotional bonding in the parent–child relationship (PBI) Gordon Parker ( Parker, 1979 ; Parker et al., 1979 ). The questionnaire consists of two scales which measure the variables “Care” and “Overcare” or “Control” by evaluating basic parenting styles through the prism of children's perception. It consists of two identical questionnaires of 25 items, one for each parent.

- Family sociogram to report its representation in the current family.

° Version of Eidemiller and Cheremisin ( Eidemiller et al., 2007 ). It is a drawing projective technique exploring several aspects: identify the position of the subject in the system of interpersonal relationships; determine the nature of communication in the family (direct or indirect). Dimensions: Number of family members who fall into the very circle; Size of the circles which mark the members; Disposition of circles (members) relative to each other (location); Distance between circles (members).

The case under study includes: demographic data of the family, anamnesis of the child (data obtained from psychological and medical research), prescribed therapy and progress, “The Time Line” ( Stanton, 1992 )—technique to retrieve significant events from the mother's history during the main stages of her development, located on the “axis of time,” data obtained from her psychological research—hers and her husband's.

N. is married with one child at 2.6 years, with suspected Autism Spectrum Disorder.

Demographic Data at First Visit

Mother (N.)—age: 36 years, education: higher, occupation: technologist.

Father (K.)—age: 39 years, education: higher, occupation: technologist.

Now, the mother is taking care of her child. Only her husband works. They live alone in a small town. The child is separated in his own room.

The child—bears his father's first name. According to parents: does not speak, does not eat independently—“He opens his mouth a little,” walks on tiptoe, does not play with other children, does not obey to commands, gets tired easily. The child attends the nursery until noon (on the recommendation of the director of the institution: “He does not eat”) and the Municipal Center for Personal Development. A social pedagogue works with him.

Data for Assessment of the Child's Development

The child was carried to full-term, born from a second, pathological pregnancy of the mother, laid in bed to avoid miscarriage in the first months. He had a protracted jaundice, which passed after a year and a half. He was not breastfed.

After a consultation with a psychologist, dysfunction was found in the following areas: Sensory: the child does not hold pelvic reservoirs, shows behavior of sensory hunger—needs intensely sensory stimuli; Motor development: with evidence of late walking, the child steps on toes; Cognitive processes: the child has not yet formed a body schema, he tends to suck the thumbs of his lower limbs; he still explores the objective world through oral modality; passivity regarding the choice of a toy if it is not in his filed vision; he does not play with his toys as intended; Emotional and social functioning: he is easily separated from the adult; the emotional expression is poorly differentiated and is played through the body by waving hands; lack of social interest; interaction is possible after prolonged sensory stimulation. Language development: he vocalizes; does not respond to his name.

During the study, the child is calm, passive. When coming into interaction, he retains his interest in the adult, but without any initiative to develop it further.

Electroencephalography was performed, in awake state and with open eyes, which displayed mixed main activity: of diffuse beta waves, and tetha waves 4.5–5 Hz, in the anterior areas: sporadically slower waves 3–4 Hz.

The child was prescribed a therapy with psychologist with live setting twice a week. The therapy with the parents was once a week. It started online prior to the beginning of the therapy with the child due to COVID-19 quarantine. Twenty sessions were held with the child, i.e., work continued for 5 weeks (with setting twice a week). The therapy includes psychological work with the child in the main areas of functioning, established as therapeutic lines of the conducted diagnostics. Ten sessions were held with the parents and the mother. Two of the sessions were held with the parents. The following were studied: their functioning through the different subsystems: marital, parental, child–parental; difficulties in raising a child with an autism spectrum. It was found that the family system organized its resource for therapy only for the child. They realized that their well-being was important for their child's development. The marital subsystem was in the background. A session was held with the father, in which his role as the Third Significant in the child's life was discussed. Seven sessions were held with the mother. In them was unfolded her personal story through early experience, child–parent relationship, main topics of growing up, intimacy, parent–child relationship with her child. The therapy is going on.

Progress of the Therapy With the Child

Decrease of sensory hunger, no tactile simulation is required to activate the child to study the objective reality; General motor skills: reduced toe walking, except in moments of agitation, he walks on a full step on a sensory path. The child jumps on tiptoe, climbing stairs is easier than getting down; Fine motor skills: improved grip (small toys, sticks, without clenching them in the fist); Cognition: recognizes himself in the mirror, experiments on dropping toys (primary circular reactions). Still uses oral inspection of some toys, beginnings of a play by designation (zone of proximal development). The active choice of toys is in progress, he explores freely the specialist room. Object constancy is formed, he seeks an object which he has played with. Lively, interesting. Emotional development: he expresses his joy by shouting and laughing, rejoices when imitated. Expresses anger. Attempts to manipulate by imitating crying. Language development: sporadically pronounces syllables, still does not respond to his name; Peculiarities: likes objects with small holes and pays lasting attention to them. He enters the oral-sadistic stage, bites toys, and gnaws some of them. Learned helplessness.

Data From Performed Psychological Studies

Child–parent relationships and internal work patterns for oneself and for the other (pbi).

The results of the self-assessment questionnaire on emotional closeness in the parent–child relationship with the mother indicate:

With reference to the relations with her mother: high results along the dimension “Overcare/Control” (24 points) and low results along the dimension “Care/Concern” (22 points). From these results it is evident that the mother in childhood is represented as emotionally cold, indifferent, and careless, and at the same time imposing control, intrusiveness, and excessive contact, infantilizing, and hindering the autonomy of N. as a child.

With reference to the relations with her father: high results along both dimensions “Overcare/Control” (32 points) and “Care/Concern” (25 points) what relates to a representation of the father's character as emotionally restrained in his behavior, but at the same time controlling, intrusive, and in attitude which is highly infantilizing and hindering the autonomy of N.

The model of adult attachment, proposed by Bartholomew and Horowitz (1991) , related through the Parker quadrant, for the emotional closeness of a child–parent shows that N. has an active negative internal work pattern for herself along the dimension of “anxiety” and is associated with vulnerability to separation, rejection, or insufficient love. The work pattern of the other is negative, associated with fear of intimacy and social avoidance, i.e., along the dimension of “avoidance.” The attachment style corresponds to style B avoidant, subcategory cowardly avoidant.

In her husband, the internal work pattern is ambivalent. The mother's character from childhood is represented as emotionally restrained and controlling, while the father's is emotionally indifferent, however encouraging autonomy.

Family Sociogram

As a child, she presented inadequate, low self-esteem, and anxiety, an experience of emotional rejection and isolation. The father was the most significant figure, he was more emotionally close. This is also observed in her relations with the maternal grandmother. The size and thickening of the circle, which it is represented with, shows high levels of intrapersonal neuroticism. There are too many figures in the circle: apart from her four-member family, mother, father, brother, and she, it also includes her maternal grandmother and her uncle, the brother of her mother, as the division is in two camps on the basis of proximity-distance: her mother, uncle, and brother are found at one end of the circle, and the other end is occupied by her, her father and grandmother.

As an adult, prior to the birth of her child, her mother was also included in the circle which is associated with a tendency to unsatisfied needs from her.

After the birth of the child, the hierarchy is maintained and there is enough space between the members of the family now.

Through the life cycle of the family and the separation/individuation, this crisis must be lived through and integrated as a new experience. The stages show that in her childhood N. did not have a sound family model, the boundaries between the parent family and the maternal family are permeable. The above configuration could be interpreted as the presence of triangulations in the family system, and as well as intergenerational ones.

Within the romantic couple, in the period of the dyad, N. presents herself and her husband in a line, as the lower part of the test field includes the figure of her mother depicted by a smaller circle. This could be interpreted with the still insufficient density of the family boundaries. Establishing family boundaries (internal and external) is an important task at this stage of family life, as well as creating an optimal balance of proximity and distance; distribution of the roles in the family; establishing the hierarchy; negotiating family rules; coordination of future life plans, as well as joint understanding and acceptance.

It is also confirmed by the results of the interpretation of the family sociogram with the father as well. As a child he presented himself with inadequate, low self-assessment, he was hierarchically placed next to the mother's figure. Prior to the birth of the child, he presented unsatisfied needs from his parental family: no separation, the boundaries between own and native family are permeable. In the present one, the experience in the reality of what is happening is available. There is no differentiation between the relationships, and dissatisfaction with them is present. The child is put in the place of unsolved contradictions.

Reflective Parenting PRFQ

In all three dimensions, the results show values above the average as IC (“interest and curiosity about mental states”) is leading-−85.5%. It is associated with intrusive hypermentalization, i.e., she is difficult to regulate and interpret her own mental states when faced with her unregulated, difficult child. As a sequence, an inadequate reaction in response to his affective signals by the mother is provoked, as well as the presence of low levels distress tolerance. In hypermentalization as a process, there is a tendency to understand or explain mental dynamics based on complex logical constructs, sometimes abstract, notional, and without pragmatic benefit. Its extreme forms are characterized by autistic, groundless fantasizing.

The possibilities for reflective parenting with the father show increased trends in the dimensions of IC (“interest and curiosity about mental states”) and CMS, which is associated with enhanced hypermentalization, as in the mother, in the cases when she does not recognize the vague mental states of her child, however, here is also a desire to understand.

In her story N. unfolds a picture of the transmission of a traumatic experience of rejection/avoidance. The experience of emotional neglect has formed a negative notion of the Self. Through her anger, she repeats the model of her mother, not realizing that her own model is possible.

N. demonstrates a personal style in which fear and anxiety constitute a centrally organizing dimension. Reported phobias are associated with behaviors of shyness, restraint, aptitude for low self-esteem, indecisiveness, uselessness, and emotional inhibition. It is difficult for her to identify anxious thoughts, as well as to connect them with their triggers from reality, to master them and to allow a “decentralized” point of view on anxious situations, what might be the birth and upbringing of a child with arrested development. Avoidance behavior is associated with a remarkably high level of distress and a low level of long-term adaptation. ( Mikulincer and Shaver, 2012 ; Lingiardi and McWilliams, 2017 ). In cognitive theory, this feature (functioning through fear and avoidance) is considered an excellent example of an early maladaptive self-assessment scheme. The theory of mentalization conceptualizes this as an implicit (automatic) mentalizing deficit. In addition, there are difficulties in understanding the mind of others ( Dimaggio et al., 2007 ; Lampe and Malhi, 2018 ). Another major deficit of mentalization is their weak affective consciousness ( Steinmair et al., 2020 ).

Mother–Child Relationship

The relationship with her child is not objective. There is no construct to include references to the related problems outlined in her child. N. includes projective identification against guild as a protective mechanism related to her wishes for the child's future. The relationship with her child is idealized, in her aspiration and strong desire for love, characteristic of her personal structure. In this case, the child serves the mother's deficits and is not perceived objectively. The projection also supports this structure in her fear of rejection. She is parenting by satisfying the child's physical needs without giving the father the opportunity to be introduced to the child's mental life. And, although the projection is central to the father, in describing the relationship with the child, their shared experiences are related to “curiosity,” “play.” The mother's fear of loss, of rejection is the result of the unprocessed mourning. It could be also thought of splitting through the non-integrated image of the early figure of attachment. Presently, she is still demonized, and the father is idealized.

In the described period the child's study of objective reality is activated. recognizable in a mirror. Demonstrates the beginning of a game as intended, expresses joy in interaction, anger. Attempts to manipulate through imitation.

Parent Couple

The possibilities for reflective parenting in both parents are associated with increased hypermentalization, and the father has a desire to understand the mental states of the child.

Married Couple

N.'s internal working models are of a cowardly avoidant style (her husband's internal working model is ambivalent). The level of adherence to therapy is low, a high level of symptom reporting, and a low level of basic confidence. Those who have a negative BPM for themselves and for the other both want and fear of intimacy in the couple. This also presupposes the future occurrence of crisis in N. married couple.

Family System

In families such as the above described, raising a child who is unable to express their own needs in a conventional way, unresolved conflicts from the beginning of their life cycle, can escalate and lead to marital dissatisfaction and dysfunction throughout the family system.

The presented integrative model of psychological support in a family raising a child with an autistic spectrum outlines a picture of improvement in two lines: in the child and in the child–parent relationship. In mother, the process of disidentification, the formation of the transmission of the object, the separation of what has been transmitted to it, allows the history of the past to be restored, therefore gives more freedom to the individual in the shaping of the individuality. Currently, the inserted traumas, even if not one's own, in the subjective experience of conflicts and fantasies, allow to integrate this experience and to turn it from destructive to structuring.

If the traumatic event is mentally processed, symbolized, and inserted in the individual memory as an experience, it receives the status of the past, of memory. It is passed on to generations not only as the content of traumatic experience but also the aptitude of its mental processing and coping with it, which affects the individual development of the child.

N.'s feedback on the therapy so far: “He showed it to us, but I, my fault, my mistake, was that I did not see it.” She finds that now is more observant.

Data Availability Statement

The datasets generated for this article are not readily available because personal data. Requests to access the datasets should be directed to Zlatomira Kostova.

Ethics Statement

Ethical review and approval was not required for the study on human participants in accordance with the local legislation and institutional requirements. Written informed consent to participate in this study was provided by the participants' legal guardian/next of kin. Written informed consent was obtained from the individual(s), and minor(s)' legal guardian/next of kin, for the publication of any potentially identifiable images or data included in this article.

Author's Note

The article presents a research perspective on the possibilities of parental capacity, through the integration of different approaches to understanding human suffering in clinical psychology.

Author Contributions

The author confirms being the sole contributor of this work and has approved it for publication.

Conflict of Interest

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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Keywords: traumatic experiences, emotional bonding, autistic spectrum disorder, family system, reflective parenting

Citation: Kostova Z (2021) Case Report: A Case Study Significance of the Reflective Parenting for the Child Development. Front. Psychol. 12:724996. doi: 10.3389/fpsyg.2021.724996

Received: 14 June 2021; Accepted: 26 July 2021; Published: 17 August 2021.

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Copyright © 2021 Kostova. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Zlatomira Kostova, z_kostova@uni-plovdiv.bg

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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• 4. Parents’ attitudes – and experiences – related to digital technology
• Acknowledgments
• Methodology

How we did this

Pew Research Center has long studied the changing nature of parenting and family dynamics as well as the adoption of digital technologies. This report focuses on how children engage with digital technologies, screens and social media, as well as parents’ attitudes about these behaviors, their concerns about their child’s use of technology, and their own assessment of their parenting and experiences with digital tech. These findings are based on a survey conducted March 2-15, among 3,640 U.S. parents who have at least one child or children ages 17 and under. This includes those who took part as members of Pew Research Center’s American Trends Panel (ATP), an online survey panel that is recruited through national, random sampling of residential addresses, as well as respondents from the Ipsos KnowledgePanel. The margin of sampling error for the full sample is plus or minus 2.2 percentage points.

Recruiting ATP panelists by phone or mail ensures that nearly all U.S. adults have a chance of selection. This gives us confidence that any sample can represent the whole U.S. adult population (see our Methods 101 explainer on random sampling). To further ensure that each ATP survey reflects a balanced cross section of the nation, the data is weighted to match the U.S. adult population by gender, race, ethnicity, partisan affiliation, education and other categories.

For more, see the report’s methodology  about the project. You can also find the questions asked, and the answers the public provided in this topline .

Parenting has never been easy. But the widespread adoption of smartphones and the rise of social media has introduced a new wrinkle to the challenges of parenthood. In fact, a majority of parents in the United States (66%) – who include those who have at least one child under the age of 18, but who may also have an adult child or children – say that parenting is harder today than it was 20 years ago, with many in this group citing technology as a reason why, according to a Pew Research Center survey conducted in March.

One of the most highly discussed – and debated – topics among parents today is screen time. How much is too much? And what impact will screens have on children’s development? Amid these growing questions, the World Health Organization issued guidelines last year on the amount of time young children should spend in front of screens.

Parents with young children themselves make clear they are anxious about the effects of screen time. Fully 71% of parents of a child under the age of 12 say they are at least somewhat concerned their child might ever spend too much time in front of screens, including 31% who are very concerned about this. 1 And some parents with a child in this age range already believe their child spends too much time on certain devices, including a smartphone. (It is important to note that this survey was fielded before the COVID-19 outbreak in the U.S. that closed many schools and led to widespread shutdowns and stay-at-home orders throughout the country.)

While a majority of parents with a young child say they are very (39%) or somewhat confident (45%) in knowing the appropriate amount of screen time for their child, they are also seeking out advice from others. Some 61% of parents of a child age 11 or younger say they have received advice or information about screen time from a doctor or other medical professional and 55% say the same about other parents, while 45% of parents of a child age 5 to 11 have turned to teachers for help.

Parents overall are also apprehensive about the long-term effects of smartphones on children’s development: 71% believe the widespread use of smartphones by young children might potentially result in more harm than benefits.

These worries come at a time when it is fairly common for children of all ages to engage – in some way – with digital devices. 2 For example, 80% of parents say their child age 5 to 11 ever uses or interacts with a tablet computer, while 63% say the same about smartphones. For parents of children under the age of 5 those shares are also notable: 48% and 55%, respectively. At the same time, roughly one-third of parents of a child 11 or younger (36%) say their child ever uses or interacts with a voice-activated assistant, like Apple’s Siri or Amazon Alexa. But there are wide age gaps: parents who have an older child, between the ages of 5 and 11 (46%), are more likely than parents with a child age 3 to 4 (30%) or 2 or younger (14%) to say their child uses or interacts with this type of technology.

Terminology

Several terms used in this report are related to parents, age of children and the technology adoption practices of children. This reference guide explains each term.

Parent is used to refer to an adult who reports being a parent or guardian of at least one child under the age of 18, but who may also have an adult child or children.

Parents of a child age 11 or younger is used to refer to parents who report having a child age 11 or younger. In cases where families have more than one child in this age range, these questions asked the parents focus on one of those children, either their oldest or youngest child in this age range (based on random assignment).

Parents of a child age 4 or younger is used to refer to parents whose randomly assigned child is under the age of 5 (0 to 4).

Parents of a child age 5 to 11 is used to refer to parents whose randomly assigned child is between the ages of 5 and 11.

Young child is used to describe children under the age of 12.

Engagement and interaction with digital technology among children was measured by asking parents about the devices their child “uses or interacts with.”

YouTube has emerged as a key platform for both younger and older kids. Fully 89% of parents of a child age 5 to 11 say their child watches videos on YouTube, as do 81% of those who have a child age 3 to 4 and 57% of those who have child age 2 or younger. And while majorities of parents whose child uses YouTube credit the platform for entertaining and educating their children, a majority of these parents are concerned about their child being exposed to inappropriate content on the video sharing site.

But the conversation around screen time is not limited to children. Parents themselves grapple with their own device distractions. When asked if they spend too much, too little or not enough time on their phone, more than half of parents overall (56%) say they spend too much time on their smartphone, while about seven-in-ten (68%) say they are at least sometimes distracted by their phone when spending time with their children.

These findings come from a nationally representative survey of 3,640 U.S. parents who have at least one child under the age of 18, but who may also have adult children, conducted online March 2-15, 2020, using Pew Research Center’s American Trends Panel and the Ipsos KnowledgePanel . The following are among the other major findings.

Many parents cite technology as a reason why parenting is harder today than in the past

When asked whether parenting is harder, easier or about the same as it was 20 years ago, larger shares of parents (66%) – which includes those who have at least one child under the age of 18 – say they believe it is harder today for most parents. Meanwhile, just 7% think it is easier, while 26% believe parenting is about the same as it was two decades ago.

Across demographic groups, parents are more likely to say that parenting today is more difficult rather than easier when compared with the past, but there are some modest differences by age. About seven-in-ten parents ages 50 and older (71%) say parenting is harder today, versus 66% of 30- to 49-year-old parents and 60% of those ages 18 to 29.

Parents cite a number of different reasons why they think parenting has grown more difficult over the years. Some of the most common responses tend to stress the impact of digital technology (26%), the rise of social media (21%) and how access to technology exposes children to things at a young age (14%). Other commonly cited reasons for parenting growing more difficult include changing morals and values and the costs associated with raising a child.

Parents are wary of the impact of mobile devices, and relatively few think children under 12 should have their own smartphone

With many children having access to mobile devices, one of the questions posed to parents and experts alike is when it is acceptable for children to have their own smartphone or tablet computer.

The ages of 12 to 14 seem to be a major milestone in parents’ eyes for smartphones. This survey finds that a majority of parents (73%) believe it is acceptable for children to have their own phone only after they have reached at least the age of 12. Some 45% say smartphone ownership is acceptable between the ages of 12 and 14, and 28% say it is acceptable between the ages of 15 and 17. Just 22% think it is OK for a child under the age of 12 to have one.

When asked about the appropriate age for a child to have their own tablet, parents are more accepting of children having one at a younger age. Fully 65% of parents say it is acceptable for child to have their own tablet computer before the age of 12.

Parents who have at least one minor child but who may also have adult children weighed in on whether they thought the use of smartphones by young children would help or hurt their ability to do a variety of things such as develop healthy friendships or do well in school. Parents are concerned about the impact that smartphones could have on children’s interpersonal skills. Fully 71% of parents say the use of smartphones by children age 11 or younger will hurt their ability to learn effective social skills a lot or a little, while a similar share says the same about developing healthy friendships. Just over half of parents think these devices will hurt children’s ability to do well in school, while parents are more evenly split when it comes to how smartphones will impact children’s ability to be creative or pursue their hobbies and interests.

YouTube is widely used by children, with parents seeing both benefits and drawbacks to the platform

Aside from interactions with the devices themselves, children also engage with a range of platforms and websites, and YouTube has emerged as a key platform for kids.

A clear majority of parents who have a child age 11 or younger say this child ever watches videos on YouTube. Among parents who say their child watches videos this way, 53% say their child does this daily, including 35% who say their child watches these videos on the platform several times a day.

But these numbers vary significantly by race and ethnicity. Black (50%) or Hispanic parents (40%) who have a child in this age range who watches YouTube are more likely to say their child does this several times a day, compared with white parents (29%).

When it comes to their opinions about the video-sharing site, parents offer both positive and negative critiques of the platform. Fully 97% of parents whose child watches videos on YouTube say it keeps their child entertained, 88% believe it helps them learn new things, while 75% say the platform exposes their child to different cultures. Still, majorities of parents are concerned about the types of videos their child may encounter on YouTube, and some report that their child has come across unsuitable material. Some 46% say their child age 11 and younger who watches YouTube videos has encountered videos that were inappropriate for their age. 3

Vast majority of parents say they limit when and how long their child can use screens, while digital ‘grounding’ is a relatively common practice for parents

In addition to parents’ concerns about screen time, there are other tech-related worries that are on their minds. Majorities of parents say they are at least somewhat concerned about their child ever being the target of online predators, accessing sexually explicit content, accessing violent content online or ever being bullied or harassed online.

Amid these worries, parents report that they monitor their young child’s digital activities in a number of ways, with most limiting screen time and using digital “grounding” as a disciplinary tactic.

Fully 86% of parents of a child age 5 to 11 say they limit the time of day or length of time their child can use screens, while eight-in-ten say they take away their child’s smartphone or internet privileges as punishment. About three-quarters of parents of a child age 5 to 11 say they check the websites this child visits or the mobile apps they use (75%) and use parental controls to restrict how much this child uses screens (72%).

Roughly half of parents of a child in this age range (49%) say they look at the call records or text messages on a smartphone used by this child. Other forms of monitoring like tracking the location of their child through GPS apps or software (33%) or friending or following their child on social media (28%) are far less common. 4

At the same time, more than half of parents of a child 11 or younger say they are at least somewhat concerned about their child ever being the target of online predators (63%), accessing sexually explicit content (60%) and accessing violent content online (59%). Somewhat similar shares (56%) report they are very or somewhat concerned that their child might ever be bullied or harassed online.

Parents have their own struggles and experiences with smartphones and social media

In addition to monitoring their children’s screen time and use of digital devices, parents also acknowledge how their own phones have led to distracted parenting.

More than half (56%) of parents who report having at least one minor child, but who may also have an adult child or children, say they spend too much time on their smartphone, while smaller shares say they spend too much time on social media (36%) or playing video games (11%).

A majority of parents also report that their phone can get in the way of spending quality time with their children. Roughly seven-in-ten parents (68%) say they are at least sometimes distracted by their smartphone, with 17% saying this happens often.

Parents’ assessments of their technology use vary by age. For example, parents ages 18 to 49 are more likely than those ages 50 and older to say they spend too much time on their smartphone (59% vs. 36%). Similarly, parents under the age of 50 are more likely than those ages 50 and older to say they often or sometimes feel distracted by their smartphone when spending time with their children (70% vs. 55%).

There are also differences by educational attainment: Parents with a college degree or higher (59%) or those with some college experience (60%) are more likely than those with a high school education or less (47%) to say they spend too much time on their smartphones. When it comes to feeling distracted by their mobile device, 75% of parents with a college degree say they are least sometimes distracted by their phone when they are spending time with their kids, compared with 68% who have some college experiences and 61% of those who have a high school education or less.

• Throughout this report there are references to parents who have children of various ages. In cases where parents have more than one child in the age ranges discussed, the parents were randomly assigned to talk about a specific child in the relevant age range. ↩
• Questions about technology adoption in Pew Research Center surveys are typically asked to the respondents directly. This survey, however, does ask parents to indicate whether or not their child engages or interacts with various digital technologies. ↩
• YouTube provides a YouTube Kids platform with enhanced parental controls and curated video playlists, but the analysis in this report focuses on YouTube as a whole. ↩
• A Pew Research Center survey conducted in 2014 and 2015 on parents of teens found some monitoring practices – like checking websites they visited and their social media profiles – to be common, while others, like using parental controls and monitoring their location with their cellphone, were less prevalent. ↩

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• Case report
• Open access
• Published: 11 September 2017

A case of a four-year-old child adopted at eight months with unusual mood patterns and significant polypharmacy

• Magdalena Romanowicz   ORCID: orcid.org/0000-0002-4916-0625 1 ,
• Alastair J. McKean 1 &
• Jennifer Vande Voort 1  

BMC Psychiatry volume  17 , Article number:  330 ( 2017 ) Cite this article

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Long-term effects of neglect in early life are still widely unknown. Diversity of outcomes can be explained by differences in genetic risk, epigenetics, prenatal factors, exposure to stress and/or substances, and parent-child interactions. Very common sub-threshold presentations of children with history of early trauma are challenging not only to diagnose but also in treatment.

Case presentation

A Caucasian 4-year-old, adopted at 8 months, male patient with early history of neglect presented to pediatrician with symptoms of behavioral dyscontrol, emotional dysregulation, anxiety, hyperactivity and inattention, obsessions with food, and attachment issues. He was subsequently seen by two different child psychiatrists. Pharmacotherapy treatment attempted included guanfacine, fluoxetine and amphetamine salts as well as quetiapine, aripiprazole and thioridazine without much improvement. Risperidone initiated by primary care seemed to help with his symptoms of dyscontrol initially but later the dose had to be escalated to 6 mg total for the same result. After an episode of significant aggression, the patient was admitted to inpatient child psychiatric unit for stabilization and taper of the medicine.

Conclusions

The case illustrates difficulties in management of children with early history of neglect. A particular danger in this patient population is polypharmacy, which is often used to manage transdiagnostic symptoms that significantly impacts functioning with long term consequences.

Peer Review reports

There is a paucity of studies that address long-term effects of deprivation, trauma and neglect in early life, with what little data is available coming from institutionalized children [ 1 ]. Rutter [ 2 ], who studied formerly-institutionalized Romanian children adopted into UK families, found that this group exhibited prominent attachment disturbances, attention-deficit/hyperactivity disorder (ADHD), quasi-autistic features and cognitive delays. Interestingly, no other increases in psychopathology were noted [ 2 ].

Even more challenging to properly diagnose and treat are so called sub-threshold presentations of children with histories of early trauma [ 3 ]. Pincus, McQueen, & Elinson [ 4 ] described a group of children who presented with a combination of co-morbid symptoms of various diagnoses such as conduct disorder, ADHD, post-traumatic stress disorder (PTSD), depression and anxiety. As per Shankman et al. [ 5 ], these patients may escalate to fulfill the criteria for these disorders. The lack of proper diagnosis imposes significant challenges in terms of management [ 3 ].

J is a 4-year-old adopted Caucasian male who at the age of 2 years and 4 months was brought by his adoptive mother to primary care with symptoms of behavioral dyscontrol, emotional dysregulation, anxiety, hyperactivity and inattention, obsessions with food, and attachment issues. J was given diagnoses of reactive attachment disorder (RAD) and ADHD. No medications were recommended at that time and a referral was made for behavioral therapy.

She subsequently took him to two different child psychiatrists who diagnosed disruptive mood dysregulation disorder (DMDD), PTSD, anxiety and a mood disorder. To help with mood and inattention symptoms, guanfacine, fluoxetine, methylphenidate and amphetamine salts were all prescribed without significant improvement. Later quetiapine, aripiprazole and thioridazine were tried consecutively without behavioral improvement (please see Table  1 for details).

No significant drug/substance interactions were noted (Table 1 ). There were no concerns regarding adherence and serum drug concentrations were not ordered. On review of patient’s history of medication trials guanfacine and methylphenidate seemed to have no effect on J’s hyperactive and impulsive behavior as well as his lack of focus. Amphetamine salts that were initiated during hospitalization were stopped by the patient’s mother due to significant increase in aggressive behaviors and irritability. Aripiprazole was tried for a brief period of time and seemed to have no effect. Quetiapine was initially helpful at 150 mg (50 mg three times a day), unfortunately its effects wore off quickly and increase in dose to 300 mg (100 mg three times a day) did not seem to make a difference. Fluoxetine that was tried for anxiety did not seem to improve the behaviors and was stopped after less than a month on mother’s request.

J’s condition continued to deteriorate and his primary care provider started risperidone. While initially helpful, escalating doses were required until he was on 6 mg daily. In spite of this treatment, J attempted to stab a girl at preschool with scissors necessitating emergent evaluation, whereupon he was admitted to inpatient care for safety and observation. Risperidone was discontinued and J was referred to outpatient psychiatry for continuing medical monitoring and therapy.

Little is known about J’s early history. There is suspicion that his mother was neglectful with feeding and frequently left him crying, unattended or with strangers. He was taken away from his mother’s care at 7 months due to neglect and placed with his aunt. After 1 month, his aunt declined to collect him from daycare, deciding she was unable to manage him. The owner of the daycare called Child Services and offered to care for J, eventually becoming his present adoptive parent.

J was a very needy baby who would wake screaming and was hard to console. More recently he wakes in the mornings anxious and agitated. He is often indiscriminate and inappropriate interpersonally, unable to play with other children. When in significant distress he regresses, and behaves as a cat, meowing and scratching the floor. Though J bonded with his adoptive mother well and was able to express affection towards her, his affection is frequently indiscriminate and he rarely shows any signs of separation anxiety.

At the age of 2 years and 8 months there was a suspicion for speech delay and J was evaluated by a speech pathologist who concluded that J was exhibiting speech and language skills that were solidly in the average range for age, with developmental speech errors that should be monitored over time. They did not think that issues with communication contributed significantly to his behavioral difficulties. Assessment of intellectual functioning was performed at the age of 2 years and 5 months by a special education teacher. Based on Bailey Infant and Toddler Development Scale, fine and gross motor, cognitive and social communication were all within normal range.

J’s adoptive mother and in-home therapist expressed significant concerns in regards to his appetite. She reports that J’s biological father would come and visit him infrequently, but always with food and sweets. J often eats to the point of throwing up and there have been occasions where he has eaten his own vomit and dog feces. Mother noticed there is an association between his mood and eating behaviors. J’s episodes of insatiable and indiscriminate hunger frequently co-occur with increased energy, diminished need for sleep, and increased speech. This typically lasts a few days to a week and is followed by a period of reduced appetite, low energy, hypersomnia, tearfulness, sadness, rocking behavior and slurred speech. Those episodes last for one to 3 days. Additionally, there are times when his symptomatology seems to be more manageable with fewer outbursts and less difficulty regarding food behaviors.

J’s family history is poorly understood, with his biological mother having a personality disorder and ADHD, and a biological father with substance abuse. Both maternally and paternally there is concern for bipolar disorder.

J has a clear history of disrupted attachment. He is somewhat indiscriminate in his relationship to strangers and struggles with impulsivity, aggression, sleep and feeding issues. In addition to early life neglect and possible trauma, J has a strong family history of psychiatric illness. His mood, anxiety and sleep issues might suggest underlying PTSD. His prominent hyperactivity could be due to trauma or related to ADHD. With his history of neglect, indiscrimination towards strangers, mood liability, attention difficulties, and heightened emotional state, the possibility of Disinhibited Social Engagement Disorder (DSED) is likely. J’s prominent mood lability, irritability and family history of bipolar disorder, are concerning for what future mood diagnosis this portends.

As evidenced above, J presents as a diagnostic conundrum suffering from a combination of transdiagnostic symptoms that broadly impact his functioning. Unfortunately, although various diagnoses such as ADHD, PTSD, Depression, DMDD or DSED may be entertained, the patient does not fall neatly into any of the categories.

This is a case report that describes a diagnostic conundrum in a young boy with prominent early life deprivation who presented with multidimensional symptoms managed with polypharmacy.

A sub-threshold presentation in this patient partially explains difficulties with diagnosis. There is no doubt that negative effects of early childhood deprivation had significant impact on developmental outcomes in this patient, but the mechanisms that could explain the associations are still widely unknown. Significant family history of mental illness also predisposes him to early challenges. The clinical picture is further complicated by the potential dynamic factors that could explain some of the patient’s behaviors. Careful examination of J’s early life history would suggest such a pattern of being able to engage with his biological caregivers, being given food, being tended to; followed by periods of neglect where he would withdraw, regress and engage in rocking as a self-soothing behavior. His adoptive mother observed that visitations with his biological father were accompanied by being given a lot of food. It is also possible that when he was under the care of his biological mother, he was either attended to with access to food or neglected, left hungry and screaming for hours.

The current healthcare model, being centered on obtaining accurate diagnosis, poses difficulties for treatment in these patients. Given the complicated transdiagnostic symptomatology, clear guidelines surrounding treatment are unavailable. To date, there have been no psychopharmacological intervention trials for attachment issues. In patients with disordered attachment, pharmacologic treatment is typically focused on co-morbid disorders, even with sub-threshold presentations, with the goal of symptom reduction [ 6 ]. A study by dosReis [ 7 ] found that psychotropic usage in community foster care patients ranged from 14% to 30%, going to 67% in therapeutic foster care and as high as 77% in group homes. Another study by Breland-Noble [ 8 ] showed that many children receive more than one psychotropic medication, with 22% using two medications from the same class.

It is important to note that our patient received four different neuroleptic medications (quetiapine, aripiprazole, risperidone and thioridazine) for disruptive behaviors and impulsivity at a very young age. Olfson et al. [ 9 ] noted that between 1999 and 2007 there has been a significant increase in the use of neuroleptics for very young children who present with difficult behaviors. A preliminary study by Ercan et al. [ 10 ] showed promising results with the use of risperidone in preschool children with behavioral dyscontrol. Review by Memarzia et al. [ 11 ] suggested that risperidone decreased behavioral problems and improved cognitive-motor functions in preschoolers. The study also raised concerns in regards to side effects from neuroleptic medications in such a vulnerable patient population. Younger children seemed to be much more susceptible to side effects in comparison to older children and adults with weight gain being the most common. Weight gain associated with risperidone was most pronounced in pre-adolescents (Safer) [ 12 ]. Quetiapine and aripiprazole were also associated with higher rates of weight gain (Correll et al.) [ 13 ].

Pharmacokinetics of medications is difficult to assess in very young children with ongoing development of the liver and the kidneys. It has been observed that psychotropic medications in children have shorter half-lives (Kearns et al.) [ 14 ], which would require use of higher doses for body weight in comparison to adults for same plasma level. Unfortunately, that in turn significantly increases the likelihood and severity of potential side effects.

There is also a question on effects of early exposure to antipsychotics on neurodevelopment. In particular in the first 3 years of life there are many changes in developing brains, such as increase in synaptic density, pruning and increase in neuronal myelination to list just a few [ 11 ]. Unfortunately at this point in time there is a significant paucity of data that would allow drawing any conclusions.

Our case report presents a preschool patient with history of adoption, early life abuse and neglect who exhibited significant behavioral challenges and was treated with various psychotropic medications with limited results. It is important to emphasize that subthreshold presentation and poor diagnostic clarity leads to dangerous and excessive medication regimens that, as evidenced above is fairly common in this patient population.

Neglect and/or abuse experienced early in life is a risk factor for mental health problems even after adoption. Differences in genetic risk, epigenetics, prenatal factors (e.g., malnutrition or poor nutrition), exposure to stress and/or substances, and parent-child interactions may explain the diversity of outcomes among these individuals, both in terms of mood and behavioral patterns [ 15 , 16 , 17 ]. Considering that these children often present with significant functional impairment and a wide variety of symptoms, further studies are needed regarding diagnosis and treatment.

Abbreviations

Attention-Deficit/Hyperactivity Disorder

Disruptive Mood Dysregulation Disorder

Disinhibited Social Engagement Disorder

Post-Traumatic Stress Disorder

Reactive Attachment disorder

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Acknowledgements

We are also grateful to patient’s legal guardian for their support in writing this manuscript.

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Magdalena Romanowicz, Alastair J. McKean & Jennifer Vande Voort

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MR, AJM, JVV conceptualized and followed up the patient. MR, AJM, JVV did literature survey and wrote the report and took part in the scientific discussion and in finalizing the manuscript. All the authors read and approved the final document.

Corresponding author

Correspondence to Magdalena Romanowicz .

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Written consent was obtained from the patient’s legal guardian for publication of the patient’s details.

Competing interests

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Romanowicz, M., McKean, A.J. & Vande Voort, J. A case of a four-year-old child adopted at eight months with unusual mood patterns and significant polypharmacy. BMC Psychiatry 17 , 330 (2017). https://doi.org/10.1186/s12888-017-1492-y

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Module 13: Disorders of Childhood and Adolescence

Case studies: disorders of childhood and adolescence, learning objectives.

• Identify disorders of childhood and adolescence in case studies

Case Study: Jake

Jake was born at full term and was described as a quiet baby. In the first three months of his life, his mother became worried as he was unresponsive to cuddles and hugs. He also never cried. He has no friends and, on occasions, he has been victimized by bullying at school and in the community. His father is 44 years old and describes having had a difficult childhood; he is characterized by the family as indifferent to the children’s problems and verbally violent towards his wife and son, but less so to his daughters. The mother is 41 years old, and describes herself as having a close relationship with her children and mentioned that she usually covers up for Jake’s difficulties and makes excuses for his violent outbursts. [1]

During his stay (for two and a half months) in the inpatient unit, Jake underwent psychiatric and pediatric assessments plus occupational therapy. He took part in the unit’s psycho-educational activities and was started on risperidone, two mg daily. Risperidone was preferred over an anti-ADHD agent because his behavioral problems prevailed and thus were the main target of treatment. In addition, his behavioral problems had undoubtedly influenced his functionality and mainly his relations with parents, siblings, peers, teachers, and others. Risperidone was also preferred over other atypical antipsychotics for its safe profile and fewer side effects. Family meetings were held regularly, and parental and family support along with psycho-education were the main goals. Jake was aided in recognizing his own emotions and conveying them to others as well as in learning how to recognize the emotions of others and to become aware of the consequences of his actions. Improvement was made in rule setting and boundary adherence. Since his discharge, he received regular psychiatric follow-up and continues with the medication and the occupational therapy. Supportive and advisory work is done with the parents. Marked improvement has been noticed regarding his social behavior and behavior during activity as described by all concerned. Occasional anger outbursts of smaller intensity and frequency have been reported, but seem more manageable by the child with the support of his mother and teachers.

In the case presented here, the history of abuse by the parents, the disrupted family relations, the bullying by his peers, the educational difficulties, and the poor SES could be identified as additional risk factors relating to a bad prognosis. Good prognostic factors would include the ending of the abuse after intervention, the child’s encouragement and support from parents and teachers, and the improvement of parental relations as a result of parent training and family support by mental health professionals. Taken together, it appears that also in the case of psychiatric patients presenting with complex genetic aberrations and additional psychosocial problems, traditional psychiatric and psychological approaches can lead to a decrease of symptoms and improved functioning.

Case Study: Kelli

Kelli may benefit from a course of comprehensive behavioral intervention for her tics in addition to psychotherapy to treat any comorbid depression she experiences from isolation and bullying at school. Psychoeducation and approaches to reduce stigma will also likely be very helpful for both her and her family, as well as bringing awareness to her school and those involved in her education.

• Kolaitis, G., Bouwkamp, C.G., Papakonstantinou, A. et al. A boy with conduct disorder (CD), attention deficit hyperactivity disorder (ADHD), borderline intellectual disability, and 47,XXY syndrome in combination with a 7q11.23 duplication, 11p15.5 deletion, and 20q13.33 deletion. Child Adolesc Psychiatry Ment Health 10, 33 (2016). https://doi.org/10.1186/s13034-016-0121-8 ↵
• Case Study: Childhood and Adolescence. Authored by : Chrissy Hicks for Lumen Learning. Provided by : Lumen Learning. License : CC BY: Attribution
• A boy with conduct disorder (CD), attention deficit hyperactivity disorder (ADHD), borderline intellectual disability.... Authored by : Gerasimos Kolaitis, Christian G. Bouwkamp, Alexia Papakonstantinou, Ioanna Otheiti, Maria Belivanaki, Styliani Haritaki, Terpsihori Korpa, Zinovia Albani, Elena Terzioglou, Polyxeni Apostola, Aggeliki Skamnaki, Athena Xaidara, Konstantina Kosma, Sophia Kitsiou-Tzeli, Maria Tzetis . Provided by : Child and Adolescent Psychiatry and Mental Health. Located at : https://capmh.biomedcentral.com/articles/10.1186/s13034-016-0121-8 . License : CC BY: Attribution
• Angry boy. Located at : https://www.pxfuel.com/en/free-photo-jojfk . License : Public Domain: No Known Copyright
• Frustrated girl. Located at : https://www.pickpik.com/book-bored-college-education-female-girl-1717 . License : Public Domain: No Known Copyright

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“My Parents Don’t Understand Me!”

About the Client:

Neha (name changed) is an 18 years old girl who belongs to a middle-class family. She has studied in a girl’s school right from her childhood. She is currently pursuing her under graduations from a renowned women’s college. She is currently in her second year. As a person, Neha is a little reserved and has a small friend circle. She takes some time to open up to people.

About Her Situation:

Neha noticed that as soon as she entered the college, there was a drastic change in her parent’s attitude towards her. According to Neha, her parents had become over-protective, suspicious, and argued with her almost on a daily basis. Her parents didn’t like her meeting school friends and especially boys and kept a check on her calls and messages. She was not at all comfortable with the restrictions her father had put on her. Neha was increasingly feeling restless and agitated. At times, she used to also answer them back which lead to further conflicts and fights. Neha was scared of her father and believed that her father would never listen to her. Neha assumed that talking to him was of no use.

Due to the constant conflicts with her parents, Neha became stressed and realised that she is not able to concentrate properly on her studies and she is lagging behind in her academics as well.

Since she was not able to deal with the situations and her studies were getting impacted really badly. That is when she decided to seek help from a counsellor .

Our Approach:

Neha came to us complaining strained relationship with her parents and constant interference from them – which are causing stress and anxiety in her. Neha and our counsellors established a working, therapeutic relationship throughout the course of the counselling sessions, following the Carl Rogers’s Client Centred Theory . Based on our initial assessment we found that Neha needed an environment where she would get the attention and acceptance so that she can express herself. Our counsellors provided an unconditional positive regard towards Neha, her beliefs, ideas, behaviours, and ways of being. This lead to catharsis following which Neha had an insight that her parents are behaving in a manner because to them she is still a kid. They are being protective and that is the reason why they are imposing too many restrictions on her.

Our counsellor helped Neha in improving her relationships with her parents. She learnt the components of healthy interpersonal relationships. She was made to think about her parent’s perspective and was asked to write it down as that might help to get a deeper understanding of the whole situation. Our counsellors encouraged her to talk to her father and our counsellors also discussed as to how her father would react to the conversations.

The Outcome:

Neha gained insight and was ready to think from her parent’s perspective. She felt fairly relived after our counselling sessions.  She also mentioned that it’s for the first time that she felt somebody understood her. She also tried initiating conversations with her parents. She worked on spending time with them, started discussing her day to day activities in college, tuitions, etc. She also began to help her mother in her daily chores which helped Neha in building a relationship with her mother and gave her the opportunity to discuss her issues. Neha mentioned that she is still not fully comfortable with her father, but with her mother, things are way better.

Neha was made to draw a timeline in which she was asked to draw/write major events from her childhood till now. Through the timeline, it was also discovered that she was once engaged in self-harming activities – slitting her wrist – but since her time in the counselling, her relationship has started to improve, and she didn’t indulge in any such activities. Neha is now doing pretty well in her academics and her relationship is improving.

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Case Report: A Case Study Significance of the Reflective Parenting for the Child Development

Affiliation.

• 1 Department of Psychology, Plovdiv University "Paisii Hilendarski, " Plovdiv, Bulgaria.
• PMID: 34512481
• PMCID: PMC8430397
• DOI: 10.3389/fpsyg.2021.724996

There are studies that connect the "child" in the past with the "parent" in the present through the prism of high levels of stress, guilt, anxiety. This raises the question of the experiences and internal work patterns formed in childhood and developed through parenthood at a later stage. The article (case study) presents the quality of parental capacity of a family raising a child with an autism spectrum. The abilities of parents (the emphasis is on the mother) to recognize and differentiate the mental states of their non-verbal child are discussed. An analysis of the parental representations for the child and the parent-child relationship is developed. The parameters of reflective parenting are measured. The methodology provides good opportunities for identifying deficits in two aspects: parenting and the functioning of the child itself. Without their establishment, therapy could not have a clear perspective. An integrative approach for psychological support of the child and his family is presented: psychological work with the child on the main areas of functioning, in parallel with the therapy conducted with the parents and the mother, as the main caregiver. The changes for the described period are indicated, which are related to the improvement of the parental capacity in the mother and the progress in the therapy in the child. A prognosis for ongoing therapy is given, as well as topics that have arisen in the process of diagnostic procedures.

Keywords: autistic spectrum disorder; emotional bonding; family system; reflective parenting; traumatic experiences.

Copyright © 2021 Kostova.

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• Published: 17 April 2024

Hybrid speciation driven by multilocus introgression of ecological traits

• Neil Rosser   ORCID: orcid.org/0000-0001-7796-2548 1 , 2   na1 ,
• Fernando Seixas   ORCID: orcid.org/0000-0002-2026-5992 1   na1 ,
• Lucie M. Queste   ORCID: orcid.org/0000-0002-7402-8079 2 ,
• Bruna Cama   ORCID: orcid.org/0000-0002-4100-9680 2 ,
• Ronald Mori-Pezo 3 , 4 ,
• Dmytro Kryvokhyzha   ORCID: orcid.org/0000-0001-6498-1977 1 , 5 ,
• Michaela Nelson 2 ,
• Rachel Waite-Hudson 2 ,
• Matt Goringe 2 ,
• Mauro Costa 6 ,
• Marianne Elias   ORCID: orcid.org/0000-0002-1250-2353 7 , 8 ,
• Clarisse Mendes Eleres de Figueiredo   ORCID: orcid.org/0000-0001-6706-7064 9 , 10 ,
• André Victor Lucci Freitas   ORCID: orcid.org/0000-0002-5763-4990 11 ,
• Mathieu Joron   ORCID: orcid.org/0000-0003-1043-4147 12 ,
• Krzysztof Kozak   ORCID: orcid.org/0000-0001-8980-3173 8 ,
• Gerardo Lamas   ORCID: orcid.org/0000-0002-3664-6730 13 ,
• Ananda R. P. Martins 14 ,
• W. Owen McMillan 8 ,
• Jonathan Ready   ORCID: orcid.org/0000-0002-9374-8661 9 , 10 ,
• Nicol Rueda-Muñoz 15 ,
• Camilo Salazar   ORCID: orcid.org/0000-0001-9217-6588 15 ,
• Patricio Salazar   ORCID: orcid.org/0000-0001-8988-0769 16 ,
• Stefan Schulz   ORCID: orcid.org/0000-0002-4810-324X 17 ,
• Leila T. Shirai 11 ,
• Karina L. Silva-Brandão 18 ,
• James Mallet   ORCID: orcid.org/0000-0002-3370-0367 1 &
• Kanchon K. Dasmahapatra   ORCID: orcid.org/0000-0002-2840-7019 2 , 19  

Nature volume  628 ,  pages 811–817 ( 2024 ) Cite this article

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• Biodiversity
• Ecological genetics
• Evolutionary genetics
• Quantitative trait loci

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species 1 , 2 . However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation 3 . Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus , which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene , and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus . These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

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Biodiversity has long been depicted as a ‘tree of life’, but a wealth of genomic data has made clear that the branches and leaves of the tree often do not represent neatly defined units. Instead, they comprise a braided delta of evolutionary lineages linked by hybridization and introgression 4 . Although gene flow tends to homogenize populations 5 , it may also contribute to adaptation and even drive speciation if introgressed variants cause reproductive isolation 1 , 2 , 6 . Polyploid (chromosome-doubling) hybrid speciation is common in plants 7 , 8 , but compelling examples of homoploid hybrid speciation (without a change in chromosome number) remain scarce and contested, especially in animals 3 . This is because it is difficult to prove that hybridization had a pivotal role in creating reproductive isolation between the hybrid lineage and the parental species 3 . Here we present evidence for homoploid hybrid speciation in Heliconius butterflies. We show that introgression of key adaptive traits from H. melpomene caused H. elevatus to diverge from H. pardalinus , despite ongoing gene flow among sympatric H. elevatus and H. pardalinus , which homogenizes 99% of their genomes (Fig. 1a ).

a , Evolutionary relationships and main introgression events described in this study. We test the hypothesis that introgression of major pre-mating and post-mating ecological isolating traits from H. melpomene led to the establishment of H. elevatus as a new stable hybrid species. Mya, million years ago. b , Geographical distributions of major clades. Locations at which both H. elevatus and H. pardalinus were sampled are numbered. c , Distance-based network using genome-wide independent SNPs. This concatenated tree shows the existence of two distinct clusters, Amazonian versus non-Amazonian, in both H. elevatus and H. pardalinus . d , Topology weighting analysis (TWISST) showing the percentage of the 11,509 non-overlapping genomic windows of 1,000 SNPs in which the majority of subtrees (that is, topology weighting ≥ 0.5) clusters H. elevatus (ele) with either H. pardalinus (par) (93.2%; top) or H. melpomene (mel) (0.52%; bottom). Note that although H. elevatus groups with H. pardalinus in 93.2% of windows, only 1.61% of those trees yield the two species as reciprocally monophyletic. By contrast, all three species are monophyletic in 81% of the windows for which H. elevatus groups with H. melpomene . Subscripts indicate geographical distributions for H. elevatus and H. pardalinus (Ama, Amazon; And, Andes; Gui, Guianas) and subspecies for H. melpomene (Agl, aglaope ; Ams, amaryllis ). e , A multispecies coalescent model with introgression supports a hybrid origin of H. elevatus , with the introgression time coinciding closely with the origin of the species (the 95% HPD intervals are given within parenthesis). Images of butterfly wings are copyright of the authors and Michel Cast.

Heliconius butterflies are chemically defended by cyanogenic glycosides, either sequestered from larval passion-vine host plants (Passifloraceae) or synthesized de novo 9 , 10 . Adults signal their toxicity to predators through their brightly coloured wing patterns. The cost of educating predators is shared with other defended butterflies and moths through mutualistic Müllerian mimicry 11 . Mimicry among species is not restricted to colour pattern, because co-mimics also converge in flight behaviour and wing shape 12 , 13 . Hybrids with intermediate phenotypes are selected against because predators do not recognize them 14 , 15 . Therefore, different mimetic phenotypes correspond to fitness peaks in an adaptive landscape maintained by disruptive selection. How populations transition to new fitness peaks remains an unanswered question, but adaptive introgression provides a possible route.

Heliconius elevatus , H. pardalinus and H. melpomene present an excellent system with which to elucidate the role of hybridization in speciation. All three species are sympatric across the Amazon basin 16 , 17 , 18 (Fig. 1b ). Heliconius elevatus and H. pardalinus are closely related 19 , but they have strikingly different colour patterns (Fig. 1a ). Heliconius pardalinus has a ‘tiger’ mimetic colour pattern typical of its close relatives. By contrast, H. elevatus has a red, black and yellow pattern, mimicking the much more distantly related H. melpomene 19 . This phenotypic convergence results in part from introgression at the major colour patterning loci cortex and optix 20 . Because Heliconius elevatus uses colour pattern as a partial cue in mate choice 17 , these introgressed alleles are likely to promote pleiotropic reproductive isolation from H. pardalinus . This suggests that H. elevatus has a hybrid origin, and here we test that hypothesis.

Hybrid genome of H. elevatus

We analysed whole-genome sequences of 92 wild-caught individuals of these three species: 42 H. elevatus (12 locations), 33 H. pardalinus (7 locations) and 17 H. melpomene (4 locations). For H. elevatus and H. pardalinus , our sampling spanned their combined geographical range (Fig. 1b and Supplementary Table 1 ). A concatenated whole-genome phylogenetic network groups H. pardalinus with H. elevatus , whereas H. melpomene forms a much deeper lineage separated by several other species 21 (Fig. 1c ). This topology is echoed in 93.2% of the genealogies estimated in sliding windows of 1,000 single-nucleotide polymorphisms (SNPs) across the genome, whereas 0.52% of the genealogies cluster H. elevatus with H. melpomene (Fig. 1d ). This is suggestive of introgression between these two species but could also be explained by retention of ancestral polymorphisms. Testing this hypothesis under the multispecies coalescent with introgression framework 22 (Fig. 1e ), we find that most of the H. elevatus genome is derived from H. pardalinus , with a 0.71% (95% high posterior density (HPD) 0.32–1.11%) contribution from H. melpomene . Heliconius elevatus arose as an independent lineage around 180,000 years ago (kya) (Fig. 1e ; 95% HPD 137–216 kya; see also Extended Data Fig. 1 ). This divergence time coincides closely with the divergence from H. pardalinus (212 kya, 95% HPD 201–224 kya) and the timing of introgression from H. melpomene (193 kya, 95% HPD 142–247 kya). These coalescent-based estimates are therefore consistent with H. elevatus being a hybrid lineage that formed through admixture between H. pardalinus and H. melpomene .

Ongoing local gene flow with H. pardalinus

Notably, the whole-genome concatenated phylogenetic network suggests that sympatric populations of H. elevatus and H. pardalinus in the Amazon are more closely related to each other than to allopatric conspecifics from the Peruvian Andes and the Guianas (Fig. 1c ). Only 1.92% (1.50% + 0.42%; Fig. 1d ) of the 11,509 windows across the genome yield reciprocally monophyletic genealogies for H. pardalinus and H. elevatus ; this is confirmed by multispecies coalescent-based trees across the genome (Extended Data Fig. 2 ). We therefore investigated whether this apparent double species paraphyly could be explained by extensive ongoing gene flow between H. elevatus and H. pardalinus in sympatry in the Amazon.

Putative natural hybrids have been reported occasionally between H. elevatus and H. pardalinus 23 , but the two very rarely mate in captivity 17 . However, F 1 hybrids from forced matings are fully fertile 17 . We therefore examined the genomes of wild-caught individuals of the two species from sympatric populations across their range for evidence of gene flow. Focusing on SNPs diagnostic for H. elevatus and H. pardalinus , we find a few individuals with long tracts of heterozygous ancestry, in some cases spanning whole chromosomes, indicating recent gene flow (Extended Data Fig. 3 ). Four-population ( f 4 ) tests comparing within- and between-species gene flow support ongoing interspecific gene flow in sympatry (Fig. 2a ). Estimated levels of effective gene flow between the species in sympatry are high ( Nm  > 1, where N is the effective population size, and m is the migration rate per generation), quite sufficient to homogenize neutral variation between species; indeed, gene flow approaches the rates that are found among nearby populations of the same species (Fig. 2b and Supplementary Table 2 ). Finally, we performed demographic modelling based on the site-frequency spectrum under different demographic scenarios and topologies. The best supported model retrieved a tree in which H. elevatus and H. pardalinus were reciprocally monophyletic, and confirmed that gene flow has been prevalent throughout their combined history (Fig. 2c and Extended Data Fig. 4 ). After their initial split, populations of H. pardalinus in the Amazon diverged from those in the Andes, and Amazonian populations of H. elevatus diverged from those in the Guianas (Fig. 2c and Supplementary Table 3 ). The two species then began to overlap broadly in the Amazon from around 28 kya (95% confidence interval 25.6–30.0 kya) until the present, with high levels of gene flow in sympatry. Nonetheless, sympatric populations of H. elevatus and H. pardalinus in the Amazon form mutually monophyletic genetic clusters (Fig. 1c ); thus, the two species remain differentiated and can clearly coexist despite extensive ongoing gene flow, implying the existence of strong sexual and ecological isolation.

a , Gene flow between species in sympatry is typically significantly greater ( f 4  > 0, filled points) than the within-species gene flow between populations across the Amazon basin. Numbers next to the points indicate the population pairs compared (see Fig. 1b ). A significant positive correlation indicates that the within-species gene flow between populations X and Y declines with increasing geographical distance relative to between-species gene flow at populations X and/or Y . b , Estimates of effective migration rate ( Nm ) within and between species using G-PhoCS. In the Amazon, between-species Nm (par Ama /ele Ama ) is similar to within-species Nm between locations (par Ama /par Ama and ele Ama /ele Ama ). The estimates for par Ama /ele Ama are denoted as filled and open circles and correspond to within and between location comparisons, respectively. c , The best supported demographic model based on the site-frequency spectrum analysis supports H. elevatus and H. pardalinus as reciprocally monophyletic (Extended Data Fig. 4 ). They initially diverged with continuous gene flow (933 to 221 kya) and after splitting into Amazonian and non-Amazonian populations, they came into secondary contact and continued exchanging genes until the present (45 kya to the present). Numbers within the blocks are effective population sizes in thousands. Arrows between groups represent continuous gene flow; numbers above or below arrows indicate 2 Nm  values.

Lack of gene flow with H. melpomene

The genome of Heliconius elevatus is, on average, more distantly related to its other parental species H. melpomene than it is to H. pardalinus (Fig. 1d and Extended Data Fig. 5a ). Yet gene flow from H. melpomene is plausible, because the latter is known to hybridize occasionally with other equally distant species in the wild 24 , 25 . None of the 31 H. elevatus or 17 H. melpomene individuals collected from areas of sympatry show any tracts of heterospecific ancestry (Extended Data Fig. 5b ). Likewise, f 4 tests do not detect any signals of gene flow (Supplementary Table 4 ). These data indicate that, in contrast to the extensive ongoing gene flow detected between H. elevatus and H. pardalinus , any recent gene flow between H. elevatus and H. melpomene is extremely rare. Because the H. elevatus and H. melpomene colour pattern phenotypes are essentially identical, this trait is probably not used to discriminate conspecifics 26 . Instead, their coexistence is likely to be due to strong assortative mating mediated by traits such as male sex pheromones and host plants (Extended Data Fig. 6 ), as well as female-limited hybrid sterility, which evolves rapidly 27 , 28 and helps to isolate H. melpomene from other sympatric, co-mimetic species 29 .

Barriers inherited from H. melpomene

As a result of extensive ongoing gene flow, differentiation ( F ST ) between sympatric populations of H. elevatus and H. pardalinus is approximately zero across around 99% of their genomes (Fig. 3 ). Only around 1% of the genome shows increased differentiation ( F ST  ≥ 0.2) and retrieves both species as reciprocally monophyletic on the basis of topology weighting by iterative sampling of subtrees (TWISST) analysis, comprising 44 genomic islands of divergence. Notably, genealogies within genomic islands resolve all populations of both species, including the peripheral allopatric lineages, as reciprocally monophyletic (Fig. 3 ). Furthermore, introgression from H. melpomene is especially prevalent in these islands and is found in 32 of the 44 genomic islands of divergence (Fisher’s exact test P  < 0.001; Fig. 3 ). Because these genomic islands resist homogenization despite gene flow in sympatry, we hypothesize that they contain the genetic basis for species differences.

Patterns of genomic divergence between sympatric H. elevatus and H. pardalinus in the Amazon together with locations of mapped traits. The black line and y axis show F ST in 25-kb sliding windows across the genome. Coloured bars show significant QTLs for different traits, with the QTL peak indicated by the triangle and the Bayesian credible intervals by the length of the bar. For colour pattern and wing shape, only QTLs with non-overlapping credible intervals are shown. Most of the genome shows very low F ST due to gene flow in the Amazon, causing the double paraphyly topology for H. elevatus and H. pardalinus in Fig. 1c . Genomic regions with rare phylogenetic topologies (bottom right) supporting introgression from H. melpomene (white circles, introgression tree) and resolving the pardalinus – elevatus species tree (grey circles, species tree) are shown above the plot. These topologies often coincide with one another and with F ST peaks. O, outgroup ( Heliconius ethilla ). FW, forewing; HW, hindwing.

To understand the genetic architecture of traits that allow the coexistence of H. elevatus and H. pardalinus , we crossed sympatric Amazonian populations of these species. We identified quantitative trait loci (QTLs) for several species-specific traits, including colour pattern, male sex pheromones, male preference for female colour pattern, wing shape, flight and female host plant preference, in F 2 and backcross offspring (Fig. 4 ). These traits contribute to reproductive isolation because they are under divergent selection and/or directly determine mate choice. For example, host preference is likely to be under divergent ecological selection and also confers non-random mating because Heliconius mate in the vicinity of their host plants 30 , 31 . In total, we identified 63 QTLs associated with species differences at these traits, which mapped to 14 of the 21 chromosomes (Fig. 3 and Supplementary Table 5 ).

a , Heliconius elevatus and H. pardalinus differ in host plant preference during egg-laying; female H. elevatus show a stronger preference for Passiflora venusta relative to Passiflora riparia . Heliconius melpomene has a very distinct host plant preference and lays eggs on neither of these plants (Extended Data Fig. 6 ). Point sizes here and in b , c are scaled by the log of sample size. Error bars are 95% confidence limits. b , The two species differ in flight dynamics; H. elevatus beats its wings significantly faster than H. pardalinus , and converges towards H. melpomene aglaope . c , Given a choice, male H. elevatus individuals preferentially court model female wings with their own colour pattern relative to H. pardalinus , whereas H. pardalinus males exhibit no preference. d , Principal component analysis (PCA) of forewing colour pattern in hybrid crosses with the parental species and H. melpomene aglaope rotated and projected into this space. Wings show the top 10% of pixels contributing to the variance in PC1. e , PCA of male sex pheromones in hybrid crosses, with parental species rotated and projected. Differences between the species are driven mainly by variance in alkanes. Selected loadings: (1) hexahydrofarnesylacetone; (2) ( Z )-9-heneicosene; (3) (Z)-11-eicosenylacetate; (4) ( Z )-9−tricosene; (5) 11-methylhexacosane; (6) 11-methylpentacosane; (7) heptacosane; (8) tricosane; (9) heneicosane (inset figure); and (10) homovanillyl alcohol. f , PCA of hindwing shape in hybrid crosses, with parental species rotated and projected. Inset wing shows changes in hindwing shape observed along PC2. Only landmarks along the margin of the wing are shown. Individual specimens are depicted as circles: H. elevatus , blue; H. pardalinus , red; F 2 s and backcrosses, grey; and H. melpomene , yellow.

QTLs for colour pattern mapped to chromosomes 1, 5, 10, 12, 13, 15 and 18, with those on chromosomes 10, 15 and 18 containing the known colour patterning genes WntA , cortex and optix (refs. 16 , 17 , 18 ). We identified a large effect locus on chromosome 20 that determined variation in hindwing shape ( H. elevatus ancestry is associated with wider and shorter hindwings). Hybrid flight dynamics were quantified using high-frame-rate video footage. A single locus on chromosome 12 predicted wing beat frequency and explained 43% of the variance. Consistent with species differences (Fig. 4b ), individuals with genotype EE (homozygous ancestry for H. elevatus ) beat their wings faster (11.2 ± 0.1 Hz) than did PP (homozygous ancestry for H. pardalinus ) individuals (10.9 ± 0.2 Hz), in which E is the H. elevatus allele and P is the H. pardalinus allele. In controlled insectary experiments, Heliconius elevatus females exhibited a strong preference for Passiflora venusta relative to Passiflora riparia (Fig. 4a ), concordant with wild host plant records 17 . A single locus on chromosome 2 predicted the preference of female hybrids for different host plants (Fig. 3 ); the probability of ovipositing on P. venusta increased from 0.3 (s.e. 0.19–0.42) for genotype PP to 0.87 (s.e. 0.81–0.91) for genotype EE.

Mate choice among sympatric populations is further mediated by female preference for male sex pheromones secreted on wing androconia and male preference for colour pattern (attractiveness of females to males) 13 . We found large effect QTLs for male androconial volatiles on chromosomes 19 and 20. These genomic regions (see Supplementary Table 5 ) contain many genes encoding enzymes that are involved in fatty acid metabolism, such as reductases and Δ9-desaturases 32 —strong candidates for controlling differences between the saturated-fatty-acid-derived androconial volatiles of H. elevatus , and the unsaturated-fatty-acid-derived blend of H. pardalinus . For example, genotype EE at the chromosome 19 locus is associated with an approximately 100-fold increase in the concentration of heneicosane, relative to genotype PP, with the QTL explaining about a third of the variance.

The male colour pattern preference QTL with the highest LOD score (3.14) was tightly linked to QTLs for androconial volatiles and wing shape on chromosome 20. However, this QTL was not statistically significant. This might be explained if male preference is highly polygenic. In support of this, we found that the probability of a male courting the H. elevatus colour pattern is positively correlated with the total fraction of the male’s H. elevatus chromosomal ancestry ( P  < 0.05, generalized linear mixed model with binomial errors and individual-level random effect). For comparison, we applied the same test to host plant choice and found no such association, suggesting that host preference has a simpler genetic basis.

Consistent with hybridization driving speciation, QTLs underpinning species-specific traits are linked to genomic windows introgressed from H. melpomene far more often than when the position of these QTLs is randomized across the genome (mean recombination rate between QTLs and nearest introgression topology, c  = 0.26; randomized mean c  = 0.39; P  < 0.001). QTL peaks that are tightly linked to H. melpomene introgression regions ( c  < 0.05) include those that determine colour pattern mimicry on chromosomes 10, 15 and 18, wing shape on chromosomes 19 and 20, male sex pheromones on chromosome 19 and 20, host plant preference on chromosome 2 and male preference on chromosome 20. Moreover, for colour pattern, wing shape, male sex pheromones and flight behaviour, H. elevatus exhibits trait values similar to those of H. melpomene (Fig. 4 ), providing a direct link between introgression, genotype and phenotype. Hence, these loci influencing ecological traits and derived from introgression represent key genomic regions that enabled hybrid speciation (Fig. 3 ).

Linkage or pleiotropy among traits are often thought to be necessary to circumvent the homogenizing effect of gene flow 5 , 33 . After removing overlapping loci in the colour pattern and wing shape phenotypic classes (Fig. 3 ), 28% of QTLs were tightly linked to at least one other species trait locus (recombination fraction c  < 0.05), and only 11% were completely unlinked ( c  ≈ 0.5). The mean recombination fraction ( c ) between trait loci and their nearest neighbour was significantly lower than when positions of the loci were randomized across the genome (observed mean c  = 0.26; randomized mean c  = 0.37; P  = 0.001). Thus, although QTLs for traits that underpin reproductive isolation are scattered across the genome, there is nonetheless significant clustering among traits. Inversions can be important for maintaining linkage disequilibria between traits that confer reproductive isolation as they suppress recombination 34 . However, with the exception of chromosome 15, in which a known inversion is associated with colour pattern differences between H. elevatus and H. pardalinus 35 , we found no candidate inversions overlapping QTL peaks (Extended Data Fig. 7 ).

Speciation was driven by introgression

The question of how new species originate and adapt to environments is fundamental to evolutionary biology. Hybridization might have a key role in establishing barriers to gene flow by creating new allelic combinations 36 , 37 . Many genomic studies have provided evidence of admixture among species 4 , 38 , 39 , 40 , 41 , but convincing cases of homoploid hybrid speciation remain scarce 1 , 3 , 6 . Here we show that H. elevatus is a hybrid species, the origin of which was triggered by introgression of traits from H. melpomene into a H. pardalinus -like ancestor (Fig. 1a ). These traits place Heliconius elevatus on a separate adaptive peak and allow it to coexist in sympatry with both parental species, despite occasional but pervasive gene flow with H. pardalinus that distorts the evolutionary history of 99% of the genome away from the species tree. Furthermore, we estimate that H. elevatus has persisted in widespread sympatry as a distinct lineage for over 720,000 generations, suggesting that it is stable and not in the process of fusing with H. pardalinus . To our knowledge, this makes it the oldest reported case of homoploid hybrid speciation, and our study is among the few to fulfil the strict criteria for hybrid speciation that were laid out in a previous study 3 . Because H. elevatus overlaps broadly across its Amazonian distribution with both progenitors, it also differs from most other previously described putative hybrid species 42 , 43 , 44 , including Heliconius heurippa 45 , which overlap with only one or neither of the parental lineages. Consistent with models of sympatric speciation 46 , traits conferring mate choice and divergent selection are clustered within the genome. Nonetheless, there are multiple clusters of these species-specific QTLs across different chromosomes. Adaptive coupling among these unlinked loci therefore spreads the effects of selection across the genome, allowing multiple genomic regions to evolve as a coadapted unit 47 , 48 , 49 , 50 , 51 . The capacity of this multilocus genetic architecture to resist gene flow indicates that sympatric speciation can occur more readily than predicted by simple theory based on small numbers of traits or loci.

Data collection and whole-genome resequencing

Collections and library preparation.

Adult butterflies were collected between 2009 and 2018 and stored at −20 °C in either salt-saturated dimethyl sulfoxide or 100% ethanol. RNA-free genomic DNA was extracted from the thorax of butterflies using Qiagen Blood and Tissue and E.Z.N.A Tissue DNA kits (Omega Bio-tek), and used to prepare 350-bp insert Illumina libraries for 33 individuals, which were sequenced using 100–150-bp paired-end sequencing on Illumina instruments. Collecting and export permit numbers are provided in the Acknowledgements. We complemented these samples with previously published sequences (see Supplementary Table 1 for sample details).

Read filtering, mapping and genotype calling

After demultiplexing, reads were filtered for Illumina adapters using cutadapt v.1.8.1 (ref. 52 ) and then mapped to the H. melpomene assembly v.2.5 (Hmel2.5, ref. 53 )(ref. 54 ) using BWA-MEM v.0.7.15 (ref. 55 ) with default parameters and marking short split hits as secondary. Mapped reads were sorted and duplicate reads removed using sambamba v.0.6.8 (ref. 56 ) sort and markdup modules, respectively. Mapped reads were further realigned around indels using the Genome Analysis Toolkit (GATK) v.3.8 RealignerTargetCreator and IndelRealigner modules 57 , 58 , to reduce the number of indel miscalls. Read depth and other relevant read alignment quality control metrics were computed using QualiMap v.2.2.1 (ref. 59 ).

Genotype calling was performed using the bcftools v.1.5 (ref. 60 ) mpileup and call modules, requiring a minimum MQ (mapping quality) and QUAL (base quality) of 20. Genotyping was performed jointly for individuals belonging to the same population using the multiallelic and rare-variant calling option (-m) in bcftools call. Ploidy aware genotype calling was performed for the Z chromosome. Genotypes were filtered using the bcftools filter module. Both invariant and variant sites were required to have QUAL (quality of the variant call) ≥ 20 and MQ (root mean square mapping quality) ≥ 20, with DP (read depth) ≥ 8 for individual genotypes (DP ≥ 4 for females on the Z chromosome) and GQ (genotype quality) ≥ 20. All genotypes not fulfilling these criteria or within 5 bp of an indel (--SnpGap) were recoded as missing data.

Species relationships and demographic modelling of hybrid speciation

Relationships between H. elevatus , H. pardalinus , H. melpomene and other closely related species were investigated by building a phylogenetic network. The dataset was filtered to include only biallelic sites (excluding singletons) without missing data and at least 1 kb apart, using Plink v.1.9 (ref. 61 ). Pairwise absolute genetic distances between all pairs of samples were calculated using the disMat.py script ( https://github.com/simonhmartin/genomics_general ). The distance matrix was then used to construct a phylogenetic network using the NeighbourNet approach 62 , implemented in SplitsTree v.4.15.1 (ref. 63 ), with default parameters.

We also investigated species relationships by estimating a concatenated neighbour-joining tree. In this analysis, we included both variable and invariable sites, at least 1 kb apart and without missing data. The neighbour-joining tree was estimated from individuals’ pairwise distances using the R package ape v.5.7 (ref. 64 ) ‘read.dna’ and ‘nj’ functions. Trees were rooted using the ‘midpoint’ function from the R package phangorn v.2.11.1 (ref. 65 ). Bootstrap supports were obtained on the basis of 100 bootstrap replicates, using the ‘boot.phylo’ function in the R package ape v.5.7 (ref. 64 ).

Genealogical relationships along the genome between the three focal species ( H. elevatus , H. pardalinus and H. melpomene ) were further investigated using TWISST 66 ( https://github.com/simonhmartin/twisst ), and using Heliconius nattereri as an outgroup species. Only SNPs fixed in the outgroup ( H. nattereri ), variable in the focal species and with a minimum allele frequency (MAF) of 0.05 were considered. Statistical phasing and imputation were performed using Beagle v.5.1 (ref. 67 ), with default settings. The phased filtered dataset was used to infer neighbour-joining phylogenies for non-overlapping windows of 1,000 SNPs (median size of around 23.6 kb), assuming the GTR substitution model, in PHYML (ref. 68 ). Exact weightings were computed for all phylogenies. Windows were classified into each of the following categories when weighting support was 0.5 or greater: (i) H. elevatus and H. pardalinus group together but are not reciprocally monophyletic; (ii) H. elevatus and H. pardalinus group together and are reciprocally monophyletic; (iii) H. elevatus and H. melpomene group together but are not reciprocally monophyletic; and (iv) H. elevatus and H. melpomene group together and are reciprocally monophyletic.

To infer the timing of introgression from H. melpomene into H. elevatus and its split from H. pardalinus , we used the multispecies coalescent-with-introgression (MSCi) model implemented in BPP v.4.6.2 (ref. 22 ) (A00 analysis). For each species of the three species, we selected four individuals to generate sequenced alignments. For H. melpomene , we used H. melpomene aglaope from Peru. Given the population structure between Amazonian and non-Amazonian population of both H. elevatus and H. pardalinus and evidence for gene flow between the two species in the Amazon, we first performed this analysis using the non-Amazonian populations (that is, H. elevatus bari and H. pardalinus sergestus ). Loci were selected randomly from autosomes, requiring loci to be 2 kb long, a minimum distance of 20 kb to the next closest locus and 5 kb from the closest exon as annotated in H. melpomene assembly v.2.5. For each locus, individuals with more than 20% missing data and sites containing missing genotype calls were removed. Only loci containing all individuals and 800 bp passing filters were considered. Heterozygous sites were assigned IUPAC ambiguity codes. Demographic parameter estimation was performed using a fixed species tree, with introgression events (see Fig. 1e and Extended Data Fig. 1 ). An inverse gamma prior (invG) was applied both to the root age ( τ 0 ) and to all populations’ effective population sizes ( θ ) – invG( a  = 3, b  = 0.06) and invG( a  = 3, b  = 0.04), respectively. A beta prior was applied to the introgression probability ( j ) – Beta( a  = 1, b  = 1). The MCMC was run for 1,000,000 iterations after 50,000 iterations of burn-in, sampling every 10 iterations.

Historic and recent gene flow

Species-diagnostic snps.

To characterize instances of recent gene flow between Amazonian H. pardalinus and H. elevatus , we relied on ancestry-informative SNPs (allele frequency difference ≥ 0.8) between these two groups. Only ancestry-informative SNPs at least 10 kb apart were considered. For each SNP, an ancestry score of 0 and 1 was assigned for H. elevatus homozygous and H. pardalinus homozygous variants, respectively, and 0.5 for heterozygous. We then calculate each individual’s ancestry (average ancestry across SNPs) and heterozygosity, on the basis of the ancestry-informative SNPs passing the filters. A custom R script was used to visualize genotypes of species-diagnostic SNPs across the genomes of different individuals. The same approach was used to determine species-diagnostic SNPs between Amazonian H. elevatus and H. melpomene .

f 4 statistics

We calculated the f 4 statistics in ADMIXTOOLS (ref. 69 ) to measure shared drift between pairs of populations of different species in the same location versus between pairs of populations of the same species in different locations. Shared drift between populations of different species in the same location is indicative of gene flow between species, and shared drift between populations of the same species in different locations is indicative of grouping by species. Only autosomal biallelic SNPs were considered in this analysis. Standard errors were estimated through a weighted block jackknife approach over 500-kb blocks. We also measured the Euclidean geographic distance between all possible pairs of locations and performed a Mantel test for its correlation with the f 4 statistics.

Estimates of gene flow between population pairs

We used G-PhoCS (ref. 70 ) to estimate divergence times, effective population sizes and migration rates between pairs of populations of H. elevatus and H. pardalinus , both within and between species. In all analyses, we also include one individual from an outgroup species ( Heliconius besckei ) and estimate model parameters assuming possible bidirectional migration between the two ingroup species. G-PhoCS uses multiple independent neutrally evolving loci to infer demographic parameters. Therefore, we first defined regions of the genome within scaffolds larger than 1 Mb and at least 1 kb away from exons as annotated in H. melpomene assembly v.2.5. Within these regions we then selected 1-kb blocks that were at least 10 kb apart from the nearest block and produced sequence alignments, masking annotated repetitive elements and CpG islands identified with the software gCluster (ref. 71 ). Because previous studies have reported extensive introgression between both H. elevatus and H. pardalinus with other Heliconius species in large regions of the genome surrounding the three major colour pattern loci, we excluded blocks in chromosomes containing these loci (chromosomes 10, 15 and 18). We also excluded blocks in the Z chromosome owing to its different effective population size. For each alignment, we excluded individuals with more than 60% missing genotype calls, and only alignments with at least three individuals per population (or all individuals in the populations for those with fewer than three individuals) and a minimum of 100 bp for which no more than 25% of individuals had missing genotype calls were considered. We coded heterozygous genotype calls using IUPAC codes. A gamma prior with α  = 2 and β  = 100 was used for both the mutational-scaled effective population size ( θ ) and the divergence time ( τ ) between the two ingroup populations, whereas a gamma prior with α  = 2 and β  = 50 was used for the divergence time to the outgroup. For the mutation-scaled migration rates, we defined a gamma prior with α  = 0.005 and β  = 0.00001. The model was run three times, with a burn-in of 50,000 iterations (allowing for automatic fine-tuning of the parameters) followed by 200,000 iterations, sampling every 200 iterations. Convergence of the Markov chain and between the three different replicates was inspected using custom scripts. To convert the θ and τ estimates to absolute effective population size and divergence time, we assumed an average mutation rate ( µ ) of 2.9 × 10 −9 substitutions per site per generation and an average generation time ( g ) of 0.25 years (ref. 72 ). We also obtain estimates of the effective migration rate ( N e m ) using the formula: N e m AB  =  M AB × θ B /4.

Simulations to infer robustness of G-PhoCS inferences

Whenever Nm  > 1, estimates of Nm for the same population comparisons varied both in value and directionality between different replicate runs of G-PhoCS. To investigate the cause for these differences, we performed coalescent simulations using MSMS (ref. 73 ). We considered the same demographic scenario as for the G-PhoCS runs; that is, two sister populations (A and B) that diverged at T D1 and split from the outgroup (C) at T D2 , and allowing either unidirectional or bidirectional migration between A and B. The split time between the two sister populations ( T D1 ) was set to four million generations, and eight million generations for the split of the outgroup ( T D2 ). An effective population size ( N e ) of one million or five million was assumed for the two ingroup populations (400,000 for the outgroup), and varying levels of gene flow ( Nm ) were considered (0.01, 0.1, 1.0, 2.0 and 10.0). For each scenario, we simulated 100 trees in MSMS (ref. 73 ), from which we generated sequence alignments using Seq-Gen v.1.3.4 (ref. 74 ). Custom scripts were used to combine pairs of haploid sequences into diploid sequences, using IUPAC codes for heterozygous sites, and to convert the alignments to the G-PhoCS sequence format. Finally, we ran G-PhoCS for the simulated datasets using the same settings as described above. Whenever Nm  > 1 in the simulated datasets, G-PhoCS showed a similar behaviour to what was seen in our analysis of the Heliconius data (Supplementary Table 6 ). We believe that this effect is due to the difficulty of estimating gene flow when the populations are nearly panmictic. Hence, for each population pairwise comparison, the highest Nm estimate among the three replicate runs is presented in Fig. 2b .

Species-tree inference

Phylogenetic relationships between the H. pardalinus and H. elevatus major groups were inferred using the multispecies coalescent (MSC) approach implemented in BPP v.4.6.2 (ref. 22 ), while accounting for incomplete lineage sorting. Three H. p. sergestus individuals (with the highest coverage) and three H. elevatus individuals from the Guianas (the individual with the highest coverage per location (French Guiana, Suriname and Venezuela)) were considered. For Amazonian H. pardalinus and H. elevatus , again, only the individual with the highest coverage from each of three locations—Ecuador, Bolivia and Brazil—was included. For this analysis, loci were selected by first defining regions of the genome within scaffolds larger than 1 Mb. To minimize the effect of linked selection, these regions also had to be at least 2 kb from exons as annotated in Heliconius melpomene v.2.5 (Hmel2.5, ref. 54 ). Because the analysis assumes no intra-locus recombination and independence between loci, we selected loci of 100–250 bp and at least 2 kb from neighbouring loci. Sequence alignments were produced for all loci, masking repetitive elements as annotated in the reference genome and CpG islands identified with the software gCluster (ref. 75 ). For each locus, individuals with more than 50% missing genotype calls were excluded from the alignment and only loci with at least two individuals per population were considered. Furthermore, sites with more than 20% of individuals with missing genotype calls were removed and loci with less than 50 bp passing filters were excluded. Loci were grouped into blocks of 100 loci, and those overlapping the inversion on chromosome 15 were grouped in a separate block. Species-tree estimation was then performed in BPP v.4.6.2 using the A01 analysis (species-tree inference assuming no gene flow). Inverse gamma priors (invGs) were applied both to the root age ( τ 0 ) and to effective population sizes ( θ ) – invG(3, 0.06) and invG(3, 0.04), respectively. Parameters were scaled assuming a mutation rate of 2.9 × 10 −9 substitutions per site per generation and a generation time of 0.25 years (ref. 54 ). The MCMC was run for 1,000,000 iterations after 50,000 iterations of burn-in, sampling every 10 iterations. Three independent runs were performed for each block, using different starting species trees, and only blocks showing consistency among the three independent runs were considered. The most abundant estimated tree across the genome showed both species to be paraphyletic with respect to each other (Extended Data Fig. 2 ). We believe that this non-taxonomic arrangement is due to gene flow, which is not accounted for in the model.

Demographic modelling by analysis of site-frequency spectra

To understand the prevalence of gene flow at different stages of the speciation history of H. elevatus and H. pardalinus , we performed demographic modelling based on analysis of the site-frequency spectrum (SFS) using fastsimcoal2 v.2.7.0.2 (ref. 76 ). For this analysis, we considered all Amazonian and non-Amazonian populations of H. elevatus and H. pardalinus . Individuals with more than 50% missing data were excluded from the analysis and only sites genotyped in at least 80% of the individuals (including all four H. p. sergestus ) were considered. Furthermore, only sites at least 2 kb apart and at least 10 kb from exons were considered, to mitigate the effects of linkage disequilibrium and linked selection, respectively. We further excluded sites within repetitive regions as annotated in the H. melpomene assembly Hmel2.5. The 209,115 sites that were retained after filtering were polarized by assessing the allele present in three outgroup species— H. besckei , Heliconius ismenius telchinia and Heliconius numata robigus . From each of the outgroup species, we chose one individual with the highest coverage and assigned the ancestral allele to each site if it was genotyped and monomorphic in the outgroup species. The unfolded multidimensional site-frequency spectrum (multiSFS) was generated using easySFS ( https://github.com/isaacovercast/easySFS ), using the recommended down projection approach (four individuals of H. p. sergestus ; 10 northeastern group H. elevatus ; and 20 H. pardalinus and 20 H. elevatus individuals from the Amazon) to maximize the number of segregating sites while accounting for missing data. For each demographic model, fitting of the simulated multidimensional site-frequency spectra to the empirical data was maximized using the composite-likelihood method implemented in fastsimcoal v.2.7 (ref. 77 ). For all model parameters, we used wide search ranges from which initial starting parameter values were randomly sampled. For each model, we performed 100 independent fastsimcoal2 runs. Parameter estimates optimization was performed for 40 expectation-maximization cycles and the expected SFS was estimated using 100,000 coalescent simulations. The best fitting model was identified by means of the Akaike information criterion, considering for each model the optimization run with the highest likelihood (using the script https://github.com/speciationgenomics/scripts/blob/master/calculateAIC.sh ). To account for stochasticity in the likelihood approximation, we further compared likelihood distributions of the different models by performing 100 independent runs from parameter values estimated under the most likely replicate run for each model. Finally, for the best fit model, confidence intervals around the maximum likelihood parameter estimates were obtained by nonparametric block-bootstrapping. For this, the 209,115 sites were divided into 100 blocks and sampled with replacement.

Genomic islands of divergence and introgression

Summary statistics.

We calculated between-population differentiation ( F ST ) for Amazonian and non-Amazonian populations of both H. elevatus and H. pardalinus groups, in sliding windows of 25 kb (5 kb step size) along the genome using the script popgenWindows.py ( https://github.com/simonhmartin/genomics_general ). The script implements a version of Hudson’s K ST (ref. 78 ), modified to avoid weighting nucleotide diversity in each population by sample size. Individuals with more than 50% missing data were removed. Only sites with a maximum of two alleles, and with at least three individuals with genotype calls per population (or the total number of individuals in populations with fewer than three individuals) were considered. Only windows with at least 10% of sites passing filters were considered in the analysis.

Topology weighting

To determine genomic regions in which H. elevatus and H. pardalinus are reciprocally monophyletic (that is, genomic regions that are potentially involved in species barriers), genealogical relationships between Amazonian and non-Amazonian populations along the genome were quantified using TWISST 66 ( https://github.com/simonhmartin/twisst ). The same dataset as for F ST was used, but also adding five individuals of representative outgroup species ( H. besckei , H. ismenius , H. numata , H. nattereri and H. ethilla ). Statistical phasing and imputation were performed using Beagle 5.1 (ref. 67 ), with default settings. Only SNPs fixed in all outgroup individuals and variable in the ingroup population with an MAF of 0.05 were considered. The phased filtered dataset was used to infer neighbour-joining phylogenies for windows of 100 SNPs (slide every 25 SNPs), assuming the GTR substitution model, in PHYML (ref. 68 ). Exact weightings were computed for all phylogenies. To estimate the proportion of trees supporting a grouping of individuals by species versus grouping by geography, we considered five groups: (i) H. elevatus from the Guianas (Venezuela, Suriname and French Guiana); (ii) H. elevatus from the Amazon; (iii) H. pardalinus from the Amazon; (iv) H. p. sergestus (Andes); and (v) an outgroup, H. nattereri . Because we hypothesize that introgression from H. melpomene into H. elevatus could be involved in speciation of the latter and H. pardalinus , the same analysis was performed including only Amazonian H. elevatus , Amazonian H. pardalinus and two H. melpomene populations ( H. m. amaryllis and H. m. aglaope ). By including H. ethilla (a sister species to H. elevatus and H. pardalinus ) as a fifth population, we were able to polarize the genealogies, allowing determination of the direction of introgression.

Association between H. melpomene introgression and genomic islands of divergence

To test whether H. melpomene introgression in the genome of H. elevatus is associated with genomic islands of divergence between sympatric H. elevatus and H. pardalinus , we performed a Fisher’s exact test. First, we defined genomic islands of divergence as regions with F ST  ≥ 0.2 and in which TWISST recovered both H. pardalinus and H. elevatus as reciprocally monophyletic (with weight ≥ 0.8). Second, we defined as introgressed, genomic regions in which TWISST grouped H. elevatus with H. melpomene with a weight ≥ 0.8. We then performed a Fisher’s exact test, as implemented in bedtools v.2.30.0 (ref. 79 ), to test whether the two sets of genomic intervals overlap more than expected given the size of the reference genome.

Genetic mapping of traits involved in reproductive isolation

Captive populations of Amazonian H. elevatus pseudocupidineus , H. pardalinus butleri and H. m. agalope were established in outdoor insectaries in Tarapoto, Peru and in heated indoor insectaries in York, UK, as previously described 17 . Crosses for QTL mapping were generated by mating H. elevatus with H. pardalinus to produce F 1 broods, and then by either crossing these amongst themselves to generate F 2 broods or backcrossing to parental taxa.

Colour pattern phenotyping

Dorsal surfaces of wings from 12 H. elevatus , 19 H. pardalinus , 14 H. m. aglaope , 348 F 2 and 50 backcross hybrids were photographed in a light box against a white background using a Canon EOS D1000 together with an X-rite ColorChecker Mini (Supplementary Table 7 ). From each image, we selected a single forewing and hindwing for analysis, clipped the image to the wing outlines and flipped wings when necessary to ensure that all were similarly orientated (resulting in two files; one forewing and one hindwing). To align the wings so that pixels represent homologous units among individuals, we used image registration 80 , a regression-based method that aligns two sets of wings (a source and a reference) according to intensity-based similarity. We chose the reference set of wings using the PCA of wing shape (see below). For forewing (36 PCs) and hindwing (26 PCs) we found the mean value for each PC across all F 2 and backcross individuals. We assigned the reference individual as the individual that had the minimum deviation from these mean values (summed across all PCs). We then checked all alignments by eye. To allow for minor misalignment or damage to wings, we included pixels in which up to 5% of individuals had missing RGB values.

Wing shape was quantified in 31 H. elevatus , 26 H. pardalinus , 10 H. m. aglaope and 308 F 2 and 36 backcross hybrids using landmark-based geometric morphometrics analyses (Supplementary Table 7 ). The ventral side of the butterfly wings was scanned using a flatbed scanner at 300 dpi and landmarks were placed at specific vein intersections 81 on the forewing (20 landmarks) and hindwing (15 landmarks) using tpsDig2 82 . Landmark coordinates were adjusted for size and orientation using a Procrustes analysis from the package geomorph 83 . Forewings and hindwings were analysed separately.

H. elevatus ( n  = 12), H. pardalinus ( n  = 13), H. m. aglaope ( n  = 5) and F 2 s ( n  = 40) were filmed flying freely in a large flight cage (5 × 2.5 × 2 m) using a GoPro HERO 4 Black camera at 239.7 frames per second at a resolution of 720p (Supplementary Table 7 ). Videos were studied in slow motion using GoPro Studio v.2.5.9.2658. Flight sequences in which an individual was flying straight and level for at least five wing beats were selected to measure wing beat frequency (WBF). WBF was measured by counting the number of complete wing beats and the number of video frames. Five WBF measurements were taken per individual from separate flight sequences and used to calculate the individuals’ mean WBF by dividing the total number of wing beats across all flight sequences by the total flight time estimated from the number of video frames.

Female host plant preference

Host plant preference assays for QTL mapping were performed by introducing single H. elevatus , H. pardalinus and F 2 females ( n  = 24, 32 and 31, respectively) into cages measuring 1 m ( W ) × 2 m ( L ) × 1.7 m ( H ), with two approximately equally sized shoots of the host plants ( P. riparia and P. venusta ) placed in the back corners. At the end of each day, the number of eggs laid on each plant species was recorded and the eggs were removed (Supplementary Table 7 ). To compare the oviposition preference of Peruvian H. elevatus , H. pardalinus and H. melpomene , groups of females (wild-caught and/or reared) of a given taxon were released into a large cage (2.5 m ( W ) × 5 m ( L ) × 2 m ( H )) containing single representatives of 21 species of Passiflora that are commonly found near Tarapoto, Peru and which represent potential host plants 17 . The number of eggs laid on each host plant was recorded at the end of each day. A total of 126 females were tested, resulting in a total of 889 eggs (176 from 35 H. elevatus females, 288 from 24 H. melpomene and 425 from 51 H. pardalinus ).

Male sexual preference

To assay male preference for female colour pattern, we presented H. elevatus , H. pardalinus and F 2 males ( n  = 46, 66 and 106, respectively) with a pair of model female wings (one H. elevatus and one H. pardalinus ), and recorded courtship events (full details of the experimental set-up are provided in ref. 17 ). Males were tested individually and placed in the experimental cage one day earlier to allow acclimatization. Trials lasted 15–30 min. The number of courtships (defined as sustained flight 5–15 cm over a model) by the males directed towards each of the model wings was recorded (Supplementary Table 7 ).

Phenotyping of androconial volatiles

Male Heliconius produce complex chemical blends of volatile compounds from their hindwing androconia. These blends have been shown to function as sex pheromones in several other Heliconius species and in butterflies in general 84 , 85 . Androconial regions were excised from 13 H. elevatus , 10 H. pardalinus , 7 H. melpomene malleti individuals and 122 F 2 and 17 backcross hybrids 21 days after eclosion, and suspended in dichloromethane. The extracts were analysed by gas chromatography–mass spectrometry (GC–MS), as reported previously 16 , 86 (Supplementary Table 7 ) on a 7890A GC-System coupled with an MSD 5975C mass analyser (Agilent Technologies) instrument fitted with an HP-5MS column (50 m, 0.25 mm internal diameter, 0.25 µm film thickness). The ionization method was electron impact with a collision energy of 70 eV. Conditions were as follows: inlet pressure 9.79 psi, He 20 ml min −1 , injection volume 1 µl. The GC was programmed as follows: start at 50 °C, increase at 5 °C min −1 to 320 °C and hold that temperature for 5 min. The carrier gas was He at 1.2 ml min −1 . For all identified compounds, the concentration was calculated from the peak’s area, as reported by AMDIS software 87 . Each compound’s chromatogram was interpreted by AMDIS through the NIST databases and the additional databases compiled at the Institute of Organic Chemistry of Technische Universität Braunschweig. All identifiable compounds running between undecane and nonacosanal were scored. Potential contaminants or extraneous compounds were excluded, together with compounds that appeared fewer than 10 times across the entire dataset.

DNA extraction and RAD library preparation for QTL analysis

RNA-free genomic DNA was extracted from thoracic tissue using a Qiagen DNeasy Blood and Tissue Kit following manufacturer’s standard protocol. Restriction-site-associated DNA (RAD) libraries were prepared using a protocol modified from (ref. 88 , using a PstI restriction enzyme, sixteen 6-bp P1 barcodes and eight indexes. DNA was Covaris sheared to 300–700 bp and gel size selected. A total of 128 individuals were sequenced per lane, with 125-bp paired-end reads, on an Illumina HiSeq 2500 (Supplementary Table 8 ).

SNP calling

Fastq files from each RAD library were demultiplexed using process_radtags from Stacks 89 , and BWA-MEM 90 was used with default parameters to map the reads to the H. melpomene assembly v.2.5 (ref. 91 ). BAM files were then sorted and indexed with Samtools (ref. 90 ), and Picard v.1.119 ( https://github.com/broadinstitute/picard ) was used to add read group data and mark PCR duplicates. To check for errors, confirm pedigrees and assign samples with unrecorded pedigree to families, we used Plink v.1.9 (ref. 61 ) to estimate the fraction of the genome that is identical by descent (IBD; \(\widehat{{\boldsymbol{\pi }}}\) ) between all pairwise combinations of samples (siblings and parent-offspring comparisons should yield \(\widehat{{\boldsymbol{\pi }}}\) values close to 0.5). In addition, for specimens that were sequenced multiple times, we checked that samples derived from the same individual \((\widehat{{\boldsymbol{\pi }}}\approx 1)\) . We then merged these samples, using the MergeSamFiles command from Picard Tools, and used Samtools mpileup command to call SNPs.

Linkage map construction

Linkage maps were built for hybrid and within-species crosses using Lep-MAP3 (ref. 92 ). Pedigrees are provided in Supplementary Table 8 . SNPs were first converted to posterior genotype likelihoods for each of ten possible SNP genotypes. We used the ParentCall2 module to correct erroneous or missing parental genotypes and call sex-linked markers using a log-odds difference of >2 (ZLimit) and halfSibs = 1. We used Filtering2 to remove SNPs showing segregation distortion, specifying a P value limit of 0.01; that is, there is a 1:100 chance that a randomly segregating marker is discarded. We then separated markers into chromosomes using their Hmel2.5 scaffold. To obtain genetic distances between markers, we fixed the order of the markers to their order in Hmel2.5, and then evaluated this order, using all markers and specifying no recombination in females. We then used map2gentypes.awk to convert the Lep-MAP3 output to four-way fully informative genotypes with no missing data. To assign ancestry to phased haplotype blocks in the hybrid linkage map, we used biallelic sites with significantly different allele frequencies in the parental species ( χ 2 test applied to sequences for 26 H. elevatus and 47 H. pardalinus individuals from Peru and Ecuador).

QTL mapping

The colour pattern, androconial volatiles and wing shape datasets are multivariate and highly collinear. We therefore used PCA to reduce the phenotypic values for the hybrids to orthogonal vectors (PCs), which we then used as phenotypes in QTL mapping. For wing shape, we applied PCA to the Procrustes coordinates. For the androconial volatiles, we applied the PCA to the set of compounds that were significantly different between the two parental species (one-tailed paired t -test). For colour pattern, we performed a PCA on the concatenated RGB values from the aligned images and retained PCs that explained more than 1% of the variance.

For colour pattern, androconial volatiles, wing shape and WBF, we tested for associations between phenotype and genotype using linear models with normal errors. For wing shape, we included centroid size as a covariate to control for allometry. For female host plant choice and male preference for female colour pattern, we (i) logistically transformed the proportions and used linear models with normal errors; and (ii) used generalized linear mixed models with an individual-level random effect to account for overdispersion and binomial errors. The significance of QTL scans was assessed by permuting the phenotypes relative to the genotypes (1,000 permutations). For traits phenotyped in both males and females, a sex-specific significance threshold was used to avoid spurious sex linkage (see Supplementary Table 5 ).

We first analysed all data using F 2 s only, using R/qtl (ref. 93 ) to estimate genotype probabilities at 1-cM intervals, using the Haldane mapping function and an assumed genotyping error rate of 0.001. These genotype probabilities were then used as the dependent variable in models, and for traits phenotyped in both males and females we included sex and cross direction as covariates for markers on the sex chromosome. For traits for which backcrosses had been scored in addition to F 2 s, we performed an additional round of analyses combining F 2 s with backcrosses. In this case, we used the categorical genotypes (EE, EP and PP) inferred from linkage mapping as the dependent variables, and added random effects for cross type (three levels: F 2 , backcross to H. elevatus , backcross to H. pardalinus ), sex or individual. Model structures and estimated coefficients are provided in Supplementary Table 5 .

To test whether QTLs are significantly clustered (that is, genetically linked), for each QTL we estimated the recombination probability with its nearest neighbouring QTLs (using the position of the maximum LOD score), and took the mean of the resulting vector (low values indicate that most QTLs are linked to at least one other QTL; high values indicate that most QTLs are unlinked). We then randomized the position of the QTLs 10,000 times and compared the observed data to the randomized dataset using a two-tailed test ( P  = the proportion of randomized datasets that give a result more extreme than the observed data × 2). When multiple QTLs overlapped within the phenotypic classes forewing colour pattern, hindwing colour pattern, forewing shape and hindwing shape, we included only the best supported QTL (highest LOD score). To test whether species and introgression topologies are associated with QTLs, we applied the same test.

To identify putative structural rearrangements between H. elevatus and H. pardalinus , we compared recombination rates between F 2 s and within-species crosses (F 2 s, 441 individuals across 26 families; H. elevatus , 179 individuals across 9 families; H. pardalinus , 296 individuals across 15 families). Regions that are freely recombining within species but not in F 2 s represent candidate rearrangements that might facilitate divergence and speciation. The probability of the within-species recombination events observed within an F 2 breakpoint can be given as p n , where p is the fraction of parental individuals in the mapping crosses and n is the observed number of recombination events. We estimated p n within each F 2 breakpoint and considered breakpoints in which p  < 0.01 to be candidate rearrangements.

Reporting summary

Further information on research design is available in the  Nature Portfolio Reporting Summary linked to this article.

Data availability

Newly generated whole-genome sequencing data used in the population genomic analyses and RAD-sequencing data used in the cross analyses have been uploaded to the NCBI Sequence Read Archive (SRA) ( PRJNA1074694 ). NCBI SRA accessions for individual samples are listed in Supplementary Tables 1 and 8 . Phenotypic data are available in Supplementary Table 7 and at https://doi.org/10.5281/zenodo.10685466 (ref. 94 ) and https://doi.org/10.5281/zenodo.10689714 (ref. 95 ).

Code availability

Custom code used for the genomic analyses ( https://github.com/FernandoSeixas/HeliconiusHybridSpeciation ) and the QTL mapping ( https://github.com/heliconius-maps/HeliconiusHybridSpeciation ) is available from GitHub.

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Acknowledgements

This work was funded by the NERC grant NE/K012886/1 to K.K.D.; a National Geographic Waitt grant (W400-15) to N.R.; grant Schu 984/12-1 from the DFG to S.S.; and Harvard University. K.K. was supported by a fellowship from the Smithsonian Institution. A.V.L.F. acknowledges support from FAPESP (2021/03868-8), from the Brazilian Research Council–CNPq (304291/2020-0) and from the USAID–US National Academy of Sciences (NAS) (AID-OAA-A-11-00012). The University of York Viking cluster high-performance computing facility was used for some of the analyses. We thank SERFOR, the Peruvian Ministry of Agriculture and the Área de Conservación Regional Cordillera Escalera (0289-2014-MINAGRI-DGFFS/DGEFFS, 020-014/GRSM/PEHCBM/DMA/ACR-CE and 040–2015/GRSM/PEHCBM/DMA/ACR-CE) for collecting permits; the Ministerio del Ambiente and Museo Ecuatoriano de Ciencias Naturales in Ecuador (005-IC-FAU-DNBAPVS/MA) for collecting permits; the ICMBio for permits (52562-3 and 10438-1); and the Conselho Nacional de Desenvolvimento Científico e Tecnológico–CNPq for approving our scientific expedition (Expediente PR no. 01300.000477/2016-49, portaria no. 4.628). This study is registered at the Brazilian SISGEN (A752FC2). Field collections in Colombia were conducted under permit no. 530 issued by the Autoridad Nacional de Licencias Ambientales of Colombia (ANLA). We thank J. Caldwell, M. Chouteau, C. Córdova, N. Edelman, S. Galluser, C. López, M. McClure, C. Pérez, C. Segami and M. Tuanama in Peru, and R. Aldaz, A. Toporov and K. Willmott in Ecuador, for help and support with fieldwork; C. Thomas, W. Valencia-Montoya, A. Kautt and J. Coughlan for comments; and M. Cast for providing some of the butterfly images used in figures.

Author information

These authors jointly supervised this work: Neil Rosser, Fernando Seixas

Authors and Affiliations

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

Neil Rosser, Fernando Seixas, Dmytro Kryvokhyzha & James Mallet

Department of Biology, University of York, York, UK

Neil Rosser, Lucie M. Queste, Bruna Cama, Michaela Nelson, Rachel Waite-Hudson, Matt Goringe & Kanchon K. Dasmahapatra

URKU Estudios Amazónicos, Tarapoto, Perú

Ronald Mori-Pezo

Universidad Nacional Autónoma de Alto Amazona, Yurimaguas, Perú

Department of Clinical Sciences, Lund University Diabetes Centre, Malmö, Sweden

Dmytro Kryvokhyzha

Residencial Las Cumbres, Caracas, Venezuela

Mauro Costa

Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC Sorbonne Universités, Muséum National d’Histoire Naturelle, Paris, France

Marianne Elias

Smithsonian Tropical Research Institute, Panama City, Panama

Marianne Elias, Krzysztof Kozak & W. Owen McMillan

Institute for Biological Sciences, Federal University of Pará (UFPA), Belém, Brazil

Clarisse Mendes Eleres de Figueiredo & Jonathan Ready

Centre for Advanced Studies of Biodiversity (CEABIO), Belém, Brazil

Departamento de Biologia Animal and Museu de Diversidade Biológica, Instituto de Biologia, Universidade Estadual de Campinas, São Paulo, Brazil

André Victor Lucci Freitas & Leila T. Shirai

Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175 CNRS, Université de Montpellier–Université Paul Valéry Montpellier–EPHE, Montpellier, France

Mathieu Joron

Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru

Gerardo Lamas

Redpath Museum, McGill University, Montreal, Quebec, Canada

Ananda R. P. Martins

Biology Program, Faculty of Natural Sciences, Universidad del Rosario, Bogotá, Colombia

Nicol Rueda-Muñoz & Camilo Salazar

Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, UK

Patricio Salazar

Institut für Organische Chemie, Technische Universität Braunschweig, Braunschweig, Germany

Stefan Schulz

Leibniz Institute for the Analysis of Biodiversity Change, Museum de Natur Hamburg Zoology, Hamburg, Germany

Karina L. Silva-Brandão

Leverhulme Centre for Anthropocene Biodiversity, Department of Biology, University of York, York, UK

Kanchon K. Dasmahapatra

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Contributions

N.R., F.S., J.M. and K.K.D designed the study. N.R. was responsible for fieldwork, including designing and conducting crosses, phenotyping of traits and performing QTL, linkage and recombination-rate analyses. F.S. performed the population genomic analyses (with D.K., N.R., J.M. and K.K.D.) and the demographic and coalescent analyses. L.M.Q. contributed to phenotyping host plant preference, colour pattern preference, wing shape, colour pattern (with B.C. and R.W.-H.) and flight (with M.G.). B.C. and S.S. led the analysis of androconial volatiles. R.M.-P. provided fieldwork assistance in Peru. M.N. constructed the RAD libraries. All other authors contributed to sample collection. N.R., F.S., J.M. and K.K.D wrote and finalized the paper with contributions from all authors.

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Correspondence to Neil Rosser or James Mallet .

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Extended data figures and tables

Extended data fig. 1 evaluating the hybrid speciation hypothesis under the msci model..

For each model, a schematic representation is depicted on top and the estimated values under the MSCi are presented in the table below. In the schematics, open circles denote internal nodes and arrows between internal nodes represent single migration pulses. Effective population sizes (N e ) are scaled to thousand individuals. The age ( τ ) of splits and nodes involved in hybridization events are given in kya. Introgression probabilities ( φ ) are depicted in blue and are given as a percentage. a , Model in which the two parental species, S (ancestral of H. melpomene ) and T (ancestral of H. pardalinus ), hybridize to originate the hybrid lineage H (ancestral of H. elevatus ), with φ contribution from parent S and 1- φ from parent T. The nodes S and T may have distinct ages and are older than node H. b , Same as model a , but constraining introgression from S into H to occur after an initial split between H. elevatus and H. pardalinus ( τ H   <   τ T ). Introgression is instantaneous and occurs at time τ H (which is the same as τ S ). c , Model allowing bidirectional migration between an H. melpomene ancestor (X) into the ancestral population of H. elevatus and H. pardalinus (Y), between an H. melpomene ancestor (S) and the lineage leading to H. elevatus (H), and between the lineage leading to H. elevatus (E) and the lineage leading to H. pardalinus (P). Note that in all models, the 95% HPD intervals of the age of gene flow from H. melpomene into H. elevatus and the split between H. elevatus with H. pardalinus overlap, in line with H. elevatus being a hybrid lineage. These are highlighted in red.

Extended Data Fig. 2 MSC analysis of H. elevatus and H. pardalinus .

Species-tree phylogeny along chromosomes calculated in blocks of 100 loci using BPP (ref. 22 ). Only the five major topologies are depicted (minor topologies are coloured in grey).

Extended Data Fig. 3 Species-diagnostic SNPs.

a , Number of species-diagnostic SNPs per chromosome. Species-diagnostic SNPs were defined as SNPs with an allelic difference of at least 0.8 between all Amazonian populations of H. elevatus and H. pardalinus . Chromosomes with at least 20 diagnostic SNPs are denoted with an asterisk (*) and shown in more detail in c . b , Triangular plot of hybrid index and observed heterozygosity, based on the 1,156 species-diagnostic SNPs, shows no evidence of early generation hybrids. c , Distribution of species-diagnostic SNPs along chromosomes in wild-caught H. elevatus and H. pardalinus . The physical location of SNPs along chromosomes (in Mb) are shown on top. Different blocks of SNPs within a chromosome, defined as groups of SNPs more than 500 kb apart, are denoted in alternating colours (black and grey). For visualization purposes, only chromosomes with at least 20 diagnostic SNPs are shown and SNP blocks were subsampled to show only one in every two SNPs. Long tracts of heterozygous genotypes (e.g. chromosome 19) suggest relatively recent hybridization followed by backcrossing.

Extended Data Fig. 4 Schematic of all demographic models tested with fastsimcoal2.

Two different tree topologies and 12 models per topology were tested. We considered the topology that retrieves both H. elevatus and H. pardalinus as monophyletic; that is, the species tree, (topology 1) and the most frequent topology across the genome (Extended Data Fig. 2 ), after excluding gene flow between H. elevatus and Amazonian H. pardalinus and in which H. p. sergestus is the first population to split (topology 2). The different demographic models are split into five main categories (depicted in different boxes): SI, strict isolation; AM, ancestral migration; SC, secondary contact; AM-SC, ancestral migration followed by secondary contact; IM, isolation with migration. Arrows between demes indicate gene flow (each direction being estimated as an independent parameter). Effective population sizes were allowed to change at split times. Note that for models under tree topology 1, the split times between H. elevatus populations and between H. pardalinus populations are different parameters and thus can assume different values.

Extended Data Fig. 5 Genetic evidence for current reproductive isolation between H. elevatus and H. melpomene .

a , Neighbour-joining tree based on autosomal sites sampled every 1 kb (166,989 sites). Values next to branches denote bootstrap values (based on 100 bootstrap iterations). Images of butterfly wings are copyright of the authors and Michel Cast. b , Distribution of species-diagnostic SNPs along chromosomes in wild-caught H. elevatus and H. melpomene . Species-diagnostic SNPs were defined as SNPs with an allelic difference of at least 0.8 between all Amazonian populations of H. elevatus and all H. melpomene populations. The physical location of SNPs along chromosomes (in Mb) are shown on top. For visualization purposes, SNP blocks were subsampled to show only 1 in every 20 SNPs. The lack of long tracts of heterozygous genotypes (or introgressed homozygous genotypes) suggests that there is no recent hybridization, followed by backcrossing, between these two species.

Extended Data Fig. 6 PCAs of male sex pheromones and host plant use show that H. elevatus , H. pardalinus and H. melpomene from the western Amazon form three distinct clusters in trait space.

a , PCA applied to concentrations of 30 male androconial volatiles. Loadings for selected compounds are annotated. b , PCA applied to oviposition preference of H. elevatus , H. pardalinus and H. melpomene for 21 species of Passiflora . Heliconius melpomene (24 females) laid 288 eggs and exhibited a strong preference for P. menispermifolia and P. triloba . Heliconius elevatus (35 females) laid 173 eggs and exhibited a preference for P. kaipiriensis . H. pardalinus butleri (51 females) laid 425 eggs and had a more generalized host plant use. To estimate the sample variance for each species, subsamples of 30 were drawn with replacement from the distribution of each species (1,000 replicates). PCA was then run on these bootstrapped replicates, polygons are minimum convex hulls encompassing all subsamples for each species. Images of butterfly wings are copyright of the authors and Michel Cast.

Extended Data Fig. 7 F ST and genetic distances plotted against physical distance.

Physical distance is shown on the x axis; grey intervals are 1 Mb and black intervals are 5 Mb. Coloured bars show significant QTLs, with the QTL peak indicated by the triangle and the Bayesian credible intervals indicated by the length of the bar. Genetic distances are estimated using three crosses—within population ( Heliconius elevatus ; elev and Heliconius pardalinus ; pard) and between population (F 2 ). Candidate inversions (CIs; indicated by black arrows) are regions that recombine within species but not in hybrids (see  Methods ). The largest CI we identified was around 1.4 Mb long at the distal end of chromosome 16. However, we identified no CIs greater than 870 kb within the credible intervals of QTLs, and only one instance of a CI that was coincident with a QTL peak (on chromosome 15). Nonetheless, some CIs outside of QTLs present compelling targets for future investigation. Notably, at the proximal end of chromosome 19 and the distal end of chromosome 16, two large CIs overlap regions with elevated F ST in which phylogenies resolve species boundaries (see Fig. 3 ).

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Rosser, N., Seixas, F., Queste, L.M. et al. Hybrid speciation driven by multilocus introgression of ecological traits. Nature 628 , 811–817 (2024). https://doi.org/10.1038/s41586-024-07263-w

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DOI : https://doi.org/10.1038/s41586-024-07263-w

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