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Evolution: Evidence and Acceptance

Ross H. Nehm ( [email protected] ) is an associate professor of science education and evolution, ecology, and organismal biology at The Ohio State University, in Columbus. His research on evolution education was recently highlighted in Thinking Evolutionarily: Evolution Education Across the Life Sciences (National Academies Press, 2012).

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Ross H. Nehm, Evolution: Evidence and Acceptance, BioScience , Volume 62, Issue 9, September 2012, Pages 845–847, https://doi.org/10.1525/bio.2012.62.9.13

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The Evidence for Evolution. Alan R. Rogers. University of Chicago Press, 2011. 128 pp., illus. $18.00 (ISBN 9780226723822 paper).

A lthough scientists view evolution as an indisputable feature of the natural world, most Americans simply do not believe that it occurs, or they reject naturalistic explanations for biotic change. Empirical studies have revealed that students and teachers often know quite a bit about evolution but still do not accept it. This somewhat counterintuitive finding has been empirically corroborated and has led science educators to investigate this pattern in order to provide suggestions for effective evolution instruction (e.g., Rosengren et al. 2012 ). Within the lucid, compact, up-to-date, and highly readable pages of The Evidence for Evolution , author Alan R. Rogers takes an approach that most science educators have found inadequate: exclusively using logic, parsimony, and the force of evidence to precipitate conceptual change about evolutionary belief. Reactions from both supportive and dissenting readers to this nicely written text will depend on how much faith they place in the use of logic to challenge the worldviews of intelligent-design creationists.

Two premises appear to frame this short book: Biology courses and textbooks are focused on evolutionary mechanisms at the expense of the evidence for evolution, which most people are not aware of, and once disbelievers of evolution are exposed to the massive amount of evidence that exists, they will change their beliefs. I am not sure whether most biologists would agree with the first premise, given the increasingly elaborate coverage of evolution in textbooks. Indeed, having reviewed some of the best-selling introductory biology books ( Nehm et al. 2009 ), I know that many topics that Rogers discusses are, in fact, covered in these texts. I am also doubtful as to whether science educators would agree with the second premise: Empirical studies have shown that learning more about evolution often fails to precipitate a meaningful belief change.

Within the 10 chapters that form the structure of The Evidence for Evolution , the choice of topics is excellent. Also noteworthy are the use of fresh empirical examples, the integration of phylogenetic trees, and the inclusion of paleontological patterns, radiometric dating, and genomic data. The evidence for evolution is vast, and choosing appropriate examples for a short book is no small task.

Writing about evolution can be quite challenging, given that many students and teachers view teleological factors as sufficient explanations for evolutionary change. It is important, therefore, to clarify what we mean when we use such language ( Rector et al. 2012 ). At times, Rogers uses intentional or teleological language: “Every living thing must solve many engineering problems just to stay alive” (p. 34). Although biologists will understand what Rogers means, the same may not be true of novice readers. Individual organisms cannot willfully change the traits that they have (e.g., they cannot intentionally modify a phenotypic feature).

Language may also invoke ideas that are at odds with current scientific thinking, and although Rogers writes with precision and clarity, some exceptions are worth mentioning. Trait loss, for example, has been shown to be a particularly difficult concept for students and teachers to understand ( Nehm and Ha 2011 ). When describing the loss of whale limbs (“Over the next few million years, whales relied less and less on their legs,” p. 20, or “Hind limbs dwindled,” p. 22), his language may be in greater alignment with common misconceptions about use and disuse than with natural selection. When writing about evolution, scientists need to be more cognizant of readers' potential interpretations of the language that we use.

One literary device employed throughout the text is the contrast of supernatural explanations (e.g., “Perhaps we sprang from the hand of God,” p. 81) with naturalistic, evolutionary explanations. Although this approach makes the text engaging, it makes little sense from my perspective and has the potential to exacerbate readers' existing confusions about core ideas relating to the nature of science (NOS). Most students and teachers remain unaware of the ontological presuppositions that undergird the scientific process (e.g., methodological naturalism). By definition (e.g., from the National Academy of Sciences), science cannot speak to or evaluate the relative merits of supernatural explanations; no amount of evidence will ever be able to tip the scale in favor of a naturalistic explanation relative to a supernatural one or vice versa. It is not clear why Rogers takes this approach.

Students' and teachers' evolutionary acceptance levels are known to be related to their understanding of the NOS. Because many Americans are deeply confused about NOS concepts such as observation , inference , testability , theory , law , model , proof , experiment , and hypothesis ( Lederman 2007 ), addressing NOS misconceptions has become de rigueur in evolution education. I was surprised, therefore, to find that The Evidence for Evolution does not discuss what evidence is or how the term is used in evolutionary science. More problematic is the somewhat careless use of NOS terms (e.g., “this experiment proved that,” p. 12, emphasis added, and “we can also see new species forming ,” p. 16, emphasis added). In order to prevent the reinforcement of such NOS misconceptions (e.g., that scientific knowledge is certain because it is proven ; or the conflation of observation and inference ), the meanings of everyday and scientific terms must be carefully distinguished for readers.

To make the most of Rogers's important contribution, pairing The Evidence for Evolution with a textbook about the NOS (e.g., Espinoza 2012 ) is much more likely to achieve what the author admirably aspires to: an understanding, acceptance, and appreciation of evolutionary science. Facts, logic, and parsimony are unlikely, on their own, to affect most people's perceptions of the plausibility of evolution.

Espinoza F . 2012 . The Nature of Science: Integrating Historical, Philosophical, and Sociological Perspectives . Rowman and Littlefield .

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Lederman NG . 2007 . Nature of Science: Past, Present, and Future . Pages 831 – 880 in Abell SK Lederman NG , eds. Handbook of Research on Science Education . Erlbaum .

Nehm RH Ha M . 2011 . Item feature effects in evolution assessment . Journal of Research in Science Teaching 48 : 237 – 256 .

Nehm RH Poole TM Lyford ME Hoskins SG Carruth L Ewers BE Colberg PJS . 2009 . Does the segregation of evolution in biology textbooks and introductory courses reinforce students' faulty mental models of biology and evolution? Evolution: Education and Outreach 2 : 527 – 532 .

Rector MA Nehm RH Pearl D . 2012 . Learning the language of evolution: Lexical ambiguity and word meaning in student explanations . Research in Science Education . Forthcoming. (3 July 2012; www.springerlink.com/content/4117121q46082l30 ) doi:10.1007/s11165-012-9296-z

Rosengren KS Brem SK Evans EM Sinatra GM eds. 2012 . Evolution Challenges: Integrating Research and Practice in Teaching and Learning about Evolution . Oxford University Press .

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Automated content analysis as a tool to compare content in sexual selection research with examples of sexual selection in evolutionary biology textbooks: implications for teaching the nature of science

• J. Kasi Jackson 1 ,
• Linda Fuselier 2 &
• Perri Eason 2  

Evolution: Education and Outreach volume  17 , Article number:  3 ( 2024 ) Cite this article

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 We used college-level evolution textbooks to examine the presentation of sexual selection research—a field with ongoing debates related to sex, sexuality and gender identity. Many classic sexual selection concepts have been criticized for androcentrism and other forms of gender-sex bias, specifically for de-emphasizing the female role in reproductive behaviors and over-reliance on gender-sex binaries. These classic concepts are fundamentally captured in the idea that animal reproductive-related behaviors can be grouped in sex roles (e.g. competitive males and selective females). Recently developed alternative concepts provide a more nuanced understanding of the flexibility of sexual and reproductive-related behaviors, stemming in part from growing attention to a broader range of female behavior. To assess whether students are receiving content reflecting these insights, we measured the congruence between textbook content and the scientific literature, using insects as a case study because of the importance of this group in the development of sexual selection theory, its prevalence in current sexual selection research, and the number of insect examples included in textbooks. We first coded textbook content for sexual selection concepts. We used automated content analysis to analyze a database of citations, keywords and abstracts in sexual selection research published between 1990 and 2014, inclusive of the period covered by the textbooks.

The textbooks and research literatures prioritized the same taxa (e.g., fruit flies) and sex roles as embodied in classic sexual selection theory. Both the research literature and some textbooks acknowledge androcentrism and other forms of gender-sex bias in classic sexual selection paradigms, especially competitive male and selective female sex roles. Yet, while the research literature included alternative models, textbooks neglected these alternatives, even when researchers had studied both classic and alternative views in the same insect.

Conclusions

 We recommend using this kind of analysis of textbook content to engage students in a conversation around the social factors that impact knowledge construction, a key part of the epistemological understanding they need for a robust grasp of the Nature of Science and of evolutionary theory.

Attempts to promote students’ understanding of the socio-scientific nature of knowledge construction, while maintaining their trust in the endeavor of science, are often framed within the context of the Nature of Science (NOS). Gender-sex and race are powerful societal, cultural, historical and biological phenomena. They are understood within complex knowledge frameworks that are challenging to capture in scientific knowledge systems. This is because those systems are often reliant on reductionist, binary-categorical, and essentialist models, which originated within racist, sexist and heteronormative frameworks (Longino 2013 ; Schiebinger 2004 ). To address this history, NOS integrates an understanding of how knowledge is shaped within simultaneously social (having to do with the interactions among scientists and within research communities) and rational (having to do with how scientists and research communities engage with their object of study) contexts. This social/rational context includes the scientific discipline and its theories and methodologies, as well as its members’ and research communities’ place within the larger society, and its attendant histories. This is manifest in the following three principles: (1) “Scientific knowledge is open to revision in light of new evidence (e.g. Scientific argumentation is a mode of logical discourse used to clarify the strength of relationships between ideas and evidence that may result in revision of an explanation);” (2) “Science is a way of knowing (e.g. Scientists’ backgrounds, theoretical commitments, and fields of endeavor influence the nature of their findings);” and (3) “Science is a human endeavor (e.g. Science knowledge has a history that includes the refinement of, and changes to, theories, ideas, and beliefs over time)” (National Research Council 2013 ). An understanding of NOS is a key ingredient in student acceptance of evolution. Specifically, students have higher acceptance of evolution when they appreciate the diversity of scientific methodologies and the nature of theory building and testing, even when controlling for interest and background in science (Lombrozo et al. 2008 ).

Understanding these NOS principles provides a foundation to challenge how science—combined with racism, sexism, heteronormativity and homophobia—maintains power differentials along presumed lines of difference. For example, eugenics—now deemed racist and sexist, among many other problems—was the mainstream and dominant research paradigm during the birth of modern evolutionary science. Scientists working within this framework were following scientific principles as they understood them, most often grounded in a positivist framework emphasizing reductionism and control. This served to maintain the status of the dominant groups, even though not all scientists at this time had this as their explicit goal (Gould 1996 ; Graves 2019 ; Subramaniam 2014 ).

Thus, teaching students about ongoing efforts to use evolutionary theory and other science either to justify or to challenge racial and other stratifications in society requires more than pointing out bias and misapplication of scientific methodologies– it must also incorporate how scientific knowledge production is intertwined with histories of racialized and gendered difference. This is especially important given the translation of scientific knowledge about human racial, sex and gender difference to the public, including biology students. For example, both interactionist and reductionist studies of hormones, sexuality and aggression have explanatory power and receive significant attention in the research community. Yet, the reductionist studies, implying that biology determines difference, have gained more coverage by the media, as well as some textbooks (Ray King et al. 2021 ). This supports an oversimplified societal narrative about hormones (biology) determining behavior that is not aligned with current scientific research (Longino 2013 ).

Although acknowledgement of the problematic history of evolutionary biology is becoming increasingly mainstream, strategies to move forward are lacking. In their absence, there has been increasing pushback and efforts to eliminate critical thinking about these issues, in large part either by banning the teaching of content that represents the current scientific consensus—especially in the area of gender-sex—or by curtailing critical frameworks that question systemic oppressions, eg critical race theory, gender studies and other critical frameworks (Rufo 2023a , 2023b ; Wallis-Wells 2021 ). The pushback against critical analyses of racism and sexism rests (1) on shifting the focus to individual identity and (2) using presumed negative impacts on these individuals, especially those from socially dominant groups, to rally support for these bans (Rufo 2023c , 2023d ; Wallis-Wells 2021 ). Thus, engaging in knowledge construction, or epistemological, frameworks that move beyond individual experience is critical.

Critical Contextual Empiricism (CCE) addresses this by framing knowledge as a communal rather than an individual pursuit (Longino 2002 ). Thus, NOS benefits from guideposts, like CCE, for navigating the social/rational processes that are included in the NOS principles, such as discourse, backgrounds, theoretical commitments, fields and histories. One CCE tenet is the argument that scientific research practices are strongest when scientific research communities are composed of more diverse groups—as long as those groups establish equitable frameworks to share and critique knowledge (Longino 2002 ). Underlying this approach is the understanding that rather than being about the identity of the individuals doing science, what is significant is their positionality, i.e. where those individuals reside in a complex matrix of identity categories and whether those with membership in these identity categories can access the power of knowledge production (Collins 2019 ). The objectivity associated with science has been privileged and historically assigned to those whose identities claim the most social, economic, and political power, leading to research outcomes supporting this division of power (Haraway 1988 ; Harding 1986 ).

CCE, coupled with the NOS principles, makes visible for students the ways in which knowledge is constructed by providing concrete examples of how scientific knowledge responds to critique. One way to capture this is to consider textbooks as a site of knowledge production, given that (1) the success of textbooks rests in their adoption by the community, and (2) they play a key role in introducing new members of the community to disciplinary norms (Bazzul 2014 ). Here we present a case study on sexual selection research on insects, which investigates how textbook content aligns with changes in research related to gender-sex, an area with changing paradigms drawn in part from larger societal and scientific discourses.

Textbooks as the Site of NOS engagement

Biology, as a research field, has begun addressing racism, sexism and heteronormativity in two ways—by attending to plasticity, variation and context when studying organisms and by acknowledging the socially constructed nature of race, gender-sex and sexuality as knowledge systems (Ah-King 2022 ; Eliot 2010 ; Fausto-Sterling 2012 ; Hyde et al. 2019 ; Lett et al. 2022 ; Montañez 2017 ; Roughgarden 2013 ; Zambrana and Williams 2022 ). Researchers have also begun to scrutinize how science textbooks address and can impact social issues related to race, gender-sex, and sexuality and gender identity (Vojíř and Rusek 2019 ).

Unfortunately, many changes in research paradigms to address racism, sexism and heteronormativity are not being transferred to the textbooks, where, outside of brief acknowledgements of past problems, textbooks often follow a strategy of avoidance (Bazzul and Sykes 2011 ; Bickford 2022 ; Donovan 2015 ). Although most include disclaimers about biology being destiny and allude to the fact that science does not provide a framework for ethical decision-making (a part of NOS), textbooks largely fail to present information to help students robustly think about race and gender-sex from a biological perspective. For example, content analyses focused on gender and sexuality found that scientific textbooks contained heteronormative assumptions (Ah-King 2013b ; Bazzul and Sykes 2011 ; Bickford 2022 ; Røthing 2017 ), gender-biased language and assumptions (Ah-King 2013b ), and gender-biased or sexist imagery (Elgar 2004 ; Good and Woodzicka 2010 ; Parker et al. 2017 ; Rosa and Gomes da Silva 2020 ; Spaulding and Fuselier 2023 ; Fuselier et al. 2018 ). In the case of race, although books are careful to challenge the idea that race is a biological construct and include evolutionary information to the contrary, they fail to challenge racism, often supported by pseudoscience, directly (Bickford 2022 ; Donovan 2015 ). For example, through a content analysis of 153 biology books (86 textbooks, 44 curricular supplements, and 23 trade books), Bickford ( 2022 ) found that although these books covered evolutionary content accurately, they did not present scientific evidence that would refute white supremacy or cis-heteronormativity. For example, Bickford ( 2022 ) found that the books often presented the lack of the validity of race as a biological construct but failed to attend to its significant role as a societal construct or to the use of science to justify racialized oppression (eg. eugenics). Overall, students lack exposure to the historical debates within biology that have led to changes in how researchers conceive of race, sex and gender as constructs in their work (reviewed in Donovan and Nehm 2020 ).

This selective or missing coverage can lead to an increase in student assumptions around biological essentialism associated with race, gender, sexuality, and gender identity. A failure to challenge social constructs of race, often grounded in pseudoscience, leads to increases in racism—even when students are then provided information intended to interrogate racialized disparities. Several studies have suggested that when biology textbooks give examples of outcomes such as diseases that are more common in one race than in others—as an attempt to address health disparities—students may develop or strengthen a belief in racial essentialism and extrapolate into other areas with racial disparities, including educational attainment (reviewed in Donovan 2015 ). To address this, Willinsky ( 2020 ) provides an overview of mixed messages about race—critiquing the falsity of race as a biological variable, while separately presenting content that uses racial groupings as a variable—in high school biology textbooks that, he argues, also reflects the how race as a concept appears in current research on race within biology. He argues that educators should integrate a historical understanding of biology’s contributions to racialized research, especially eugenics, and use the contradictory messaging present within textbooks to demonstrate the complexities of conducting research on systemic racism and racialized outcomes in health and other biological fields (Willinsky 2020 ).

Similar findings hold for beliefs about gender and sex difference. Donovan et al. ( 2019a ) investigated the impact when 8th-10th grade students read selections from biology textbooks on the students’ belief in a neurogenetic basis for sex differences in humans and interest in science. They compared a passage refuting neurogenetic sex differences with two passages endorsing neurogenetic differences—one in humans and one in plants. Students self-identifying as girls who read the endorsing passages, whether in plants or humans, were more likely to believe in sex differences grounded in neurogenetics; girls in these treatments also indicated less interest in science. A further examination of student writing after reading the passages indicated that students tended to use both sex and gender language in all treatments, with some evidence that they were distinguishing between the concepts to refute essentialism in the refutational text treatment (Stuhlsatz et al. 2020 ). Recognizing that biology textbooks also conflate biological sex differences with gendered social outcomes, the authors recommend an approach emphasizing the complex histories of science research on both sex and gender, accompanied by training for teachers on how to address this content with their students. Our study aims to provide such a resource in the case of sexual selection.

Sexual selection and changing paradigms

One area in which scientific research and other scholarly work have begun to address at least some gender-biased assumptions is sexual selection research (Ah-King 2022 ; Ah-King and Ahnesjö, 2013 ). In our previous work, we found that although some evolutionary biology textbooks acknowledge the critique of gender bias in scientific research, their presentation of sexual selection research in text, and especially in images, retains an emphasis on the work that has been critiqued for said gender-sex bias (Fuselier et al. 2016 , 2018 ). This also occurs in animal behavior textbooks, which devote more space to sexual selection (Spaulding and Fuselier 2023 ).

Although sexual selection is typically covered in evolution courses, little research has been done to ascertain how it is taught and how students understand it (Ziadie and Andrews 2018 ). Sexual selection research originated as a study of extreme differences between males and females, e.g. strong sexual size dimorphisms or other traits that occur or are highly exaggerated in only one sex, such as the classic example of the peacock’s ornamental tail. The classic view of sexual selection emphasizes stable binary sex roles with males competing, either by fighting with other males or by displaying to females who may choose the males as mates based on their displays or dominance over other males. The roles may be reversed, with female competition for mates, given changes in the environment, such as restricted nesting sites, resulting in more female animals ready to mate than have access to resources needed for mating —but this phenomena was seen to support the existence of the binary itself (Ah-King and Ahnesjö, 2013 ; Trivers 1976 ).

Feminist critiques of androcentric bias in sexual selection theory began soon after its publication (Blackwell 1875 ; Hamlin 2015 ), and work critiquing androcentric bias and offering solutions has been ongoing in the field ever since (reviewed in Jackson 2001a , b , 2014 ). After the 2000’s, the frequency of such research in mainstream animal behavior and evolution journals has increased (reviewed in Fuselier et al. 2016 ). The field has been critiqued most often for importing assumptions about human sex roles into the study of non-human organisms (e.g. Hrdy 1986 ). Additional ongoing areas of concern include acknowledging the context-specific nature of sexual behavior and mating patterns (Gowaty 2013 ; Kokko and Johnstone 2002 ), though the extent of the challenge to traditional notions of sexual selection is a subject for debate (see for example the exchange between Ah-King 2013a ; Kokko et al. 2013 ). Researchers in sexual selection have acknowledged the lack of studies of female organisms (Clutton-Brock 2009 ) and have highlighted not only sexual selection on females but also several alternative behaviors that expand the classic understanding of sexual selection, such as male mate choice, female ornaments, male parental care, female-female competition and flexible sex roles (reviewed in Fuselier et al. 2016 ).

College-level evolutionary biology textbooks present primarily classic sexual selection binary sex-role theory, although some textbooks do present some examples of alternatives to classic roles, most commonly extra-pair copulations and polyandry—situations in which female animals mate with multiple males (Fuselier et al. 2016 ). Yet, the images included in the textbooks display a more conservative representation of classically understood sex roles than the content covered in the writing (Fuselier et al. 2018 ). It is unclear how the content presented in textbooks reflects the scientific literature. One challenge to research in this area is the difficulty of synthesizing the vast amounts of information available in the literature for comparison with the textbooks, a necessity for making recommendations for how to modify content or examining how the instructor frames what the books do—or, more importantly, fail to do. Here we explore the efficacy of automated content analysis (ACA) as a tool to assess the alignment of textbook content with the scientific literature.

Automated content analysis (ACA) essentially turns text into data, using sets of algorithms to construct models that allow researchers to determine the concepts on which authors focus, as well as the relationships among those concepts. ACA has been used recently to assess and identify trends and shifts in ecology and evolutionary biology (Nunez-Mir et al 2016 ; McCallen et al. 2019 ). Essentially, ACA programs based on machine-learning (ML) identify words or word combinations that are commonly associated with one another in text by determining how frequently they co-occur in small blocks of text (3–4 lines) versus how frequently they occur elsewhere. Leximancer does not use a training set like other artificial intelligence programs might; more information about algorithms used in the program is reviewed in Smith and Humphreys ( 2006 ). Through machine learning, ACA identifies and quantifies the associations of terms to develop a thesaurus and create “concepts” and groups of concepts related to the same theme. The frequency of and relationships among concepts and themes can be calculated, assessed, and visualized. The power of this type of analysis is the large amount of literature (or text) that can be assessed in a relatively short time. ACA is thus an excellent tool for comparing the content of textbooks to the topics emphasized within the literature on a given subject. It can reveal how researchers address particular topics both currently and over time, as well as gaps or lags in textbooks’ coverage of a field.

We used insects as a proof of concept for the ML-based ACA technique because our prior research demonstrated that a wider range of sexual selection roles was presented in this taxon than in any other group used in the textbooks (Fuselier et al. 2016 ). After completing analysis of the peer-reviewed articles, we then compared all the concepts that were studied in insects to the concepts that textbooks used these insects to exemplify. We also examined whether the insects used to represent specific behaviors in textbooks reflected the insect taxa in which these behaviors were most studied in the peer-reviewed articles. We addressed the following specific research questions:

What sexual selection behaviors are studied in insect taxa in peer-reviewed literature?

Do the insect taxa described in textbook discussions of sexual selection match the insect taxa studied in peer-reviewed articles in the sexual selection literature?

How does the range of sexual selection behaviors covered in textbooks compare to the range of behaviors discussed in peer-reviewed articles?

We used four recent evolutionary biology textbooks (Table  1 ) published between 2012 and 2013 that in 2016 represented over 95% of the market share of college-level evolution textbooks in the United States. The textbooks were the same used in our prior research (Fuselier et al. 2016 , 2018 ).

We created an inventory of all insects used as examples in textbook sections devoted to sexual selection topics. The examples were classified as fitting into one of two understandings of sexual selection: classic (e.g., male-male competition, female choice) or expanded (e.g., competition among females, reproductive constraints among males, or mate choice as a mutual process).

Literature search and dataset

To construct a literature database, we used the Zoological Record collection within Web of Science (Clarivate Analytics) to identify proceedings, peer-reviewed journal articles, books and book chapters focused on sexual selection in insects. We focused on the Zoological Record because this database is the oldest database focused on animal science and is known for its focus on zoology and animal biology. It covers international journals on behavior, with an emphasis on knowledge pertinent to the study of non-human animals in the wild; it thus contains the literature most relevant to our study (Zoological Record​ on Web of Science 2024 ). Its organization by taxonomy also mirrors our study’s emphasis on taxonomic differences, and thus its structure was particularly amenable to the ways that we needed to sort the literature to answer our research questions. We limited our search to the years 1990–2014, dates for which we were able to access abstracts for the papers. This period marks a significant time frame for a renewal of interest in sexual selection, and an associated feminist critique of androcentric bias. Given that the latest publication date of our selected books was 2013, it also included the literature most likely to be covered in the books and thus ensured that the records were those most pertinent to our research questions.

We constructed our search using Boolean operators, identifying papers with topics including both ‘sexual selection’ and ‘insect’ or its variants (e.g., insects, Insecta). After reviewing the literature, we realized that this search also included research in which the insect was not the focus of the study, e.g., studies on sexual selection in flowers mediated by insect pollinators, and studies of the impacts of sexual selection on bird traits in which the traits were signaling resistance to an insect parasite. To remove these studies, we added a supertaxon search term to search separately for papers in which the supertaxon was or was not Insecta. Most studies identified by this revised search were those with the supertaxon Insecta, and all of these (n = 1581) focused on sexual selection in insects. In a smaller set of studies (n = 105), the supertaxon was not Insecta. We reviewed these manually and removed 52 publications that did not focus on sexual selection in insects. The remaining 53 papers, which did cover sexual selection in insects, were often reviews or comparative studies in which sexual selection in an insect was being compared to sexual selection in another taxon, e.g., studies comparing nuptial gifts in spiders (Arachnida) versus crickets (Insecta). These papers were included in our final dataset of 1634 papers.

We then imported the full records (including full citations, abstracts, automatic tags, and other metadata) into a database. We manually reviewed the 1634 records to sort them into our final taxonomic groupings. This resulted in nine groups, which included seven insect orders, the genus Drosophila (fruit flies), and an ‘other’ group that included all taxa that were the focus of fewer than 20 studies each. We separated Drosophila from its parent taxon Diptera (flies) because of the large number of studies on Drosophila ; there were more studies on Drosophila than on any other group (Table  2 ). We then exported these to Microsoft Excel © for automated content analysis.

• Automated content analysis

We analyzed spreadsheets containing article titles, abstracts and manual search terms for the nine groups of insect taxa using Leximancer, a machine-learning-based program for automated content analysis (Leximancer 2019 ). To identify the most commonly studied topics in sexual selection in insects among the 1634 papers, we used an “overall” analysis of concepts in which we allowed the program to find concepts and build a thesaurus from automatically generated terms. For a second, “profiled” analysis we added “user-defined concepts” specifically related to alternatives to classic sex roles such as polyandry, mutual mate choice, alliances, etc. To verify that user-defined concepts aligned with the meaning in the text, an investigator checked the meaning in the text with the excerpts identified by the program. For example, using the compound term “female + competition” when searching for papers that addressed competition among females for mates, text excerpts that contained the two words in a sentence but did not refer to female competition were excluded (e.g., “competition experiments…showed males mated with more females”). We modified the compound concepts (e.g., “female + competition + NOT male”) and re-ran analyses until we minimized the occurrence of inaccurate matches with the text. We used measures (produced by Leximancer ® ) of the frequency and strength of association to identify what topics were most commonly studied among which taxa; we used prominence values to quantify the relationship between taxa and topic. Prominence is a combination of strength and frequency within a taxon, and prominence values > 1 indicate that the association happens more often than expected by chance.

1) What sexual selection behaviors are studied in insect taxa in peer-reviewed literature?

Overall analysis

The overall analysis identified 64 commonly occurring concepts (see Table  3 and Appendix A). The concept ‘male’ was the most commonly encountered concept in the dataset, and thus was more common than ‘female.’ Examination of the concepts most frequently co-occurring with the five top concepts revealed that research on sexual selection in insects has emphasized males over females and focused on post-copulatory selection, communication (e.g., calling), and biometrics, among other topics. All taxa had a high frequency of association with the concepts, meaning that given the taxon, we were highly likely to find papers that included the concept. But, given the concept, the strength of association with a particular taxon was low, indicating that all the commonly encountered concepts were studied in all taxa. Interestingly, the concept ‘female’ occurred most often in association with the concept ‘re-mating’ and, secondly, ‘choice.’ Re-mating was used in studies of conflict, which was one of the top associations with the term ‘sexual,’ indicating that there is a wealth of literature on sexual conflict and that it includes an examination of females re-mating, which is one of the expanded views of sexual selection because it emphasizes multiple mating by females.

Profiled analysis

In this analysis we removed very general concepts, (e.g., male, female, sexual, evolution, behavior, reproduction, and variation) that were studied in all taxa and included 16 user-defined concepts that emphasized alternatives to classic sexual selection. Removing general concepts provided the opportunity to examine more closely which insects were used to study expanded sexual selection. For example, the sheer number of studies on speciation in fruit flies impeded the program’s ability to detect associations of fruit flies with non-traditional concepts (e.g., condition-dependent mate choice).

Four of the nine taxonomic groups were strongly and frequently associated with particular expanded concepts (Table  4 ): beetles, fruit flies, butterflies/moths, and flies. Beetles and fruit flies were frequently associated with concepts related to sperm competition and conflict (sperm competition, male costs, sperm storage, conflict, polyandry, and multiple female mating). Fruit flies, beetles and crickets were associated with condition-dependent mate choice, male mate choice and female aggression. Finally, butterflies/moths were associated with female signals, mainly pheromones, and flies were associated with conflict.

Overall, expanded concepts were studied in many insect taxa, and all expanded concepts appeared prominently in two or more taxonomic groups. On average, for each concept (e.g., “female ornaments”) there were three taxa with significant prominence values. The most infrequently studied expanded concept was female reproductive success, which was only prominently associated with beetles and butterflies/moths. Beetles and fruit flies were central to the studies of expanded concepts of sexual selection. Although studies using fruit flies made up the largest proportion of papers we identified for our dataset, more expanded concepts (n = 10) were significantly prominent in beetles than in fruit flies (n = 8).

Comparison to textbooks

2) Do the insect taxa described in textbook discussions of sexual selection match the insect taxa studied in peer-reviewed articles in the sexual selection literature?

Overall, fruit flies, beetles and crickets/grasshoppers were the most commonly studied groups in the scientific literature (Table  5 ). All flies (Diptera) including fruit flies accounted for 31% of the experimental science studies. This matches well with the proportions of examples used across all textbooks combined for flies, which was also 31%. However, when we looked at individual textbooks, the proportion of examples that used fruit flies or flies ranged from 16 to 50%, with one textbook (Pearson, 33%) matching the distribution of taxa in the literature but the others with far greater or lower representation than expected based on the literature.

3) How does the range of sexual selection behaviors covered in textbooks compare to the range of behaviors discussed in peer-reviewed articles?

The profiled analysis showed that most of the alternatives to traditional sex roles were covered in two taxonomic groups—fruit flies and beetles. Therefore, if the textbooks are covering these alternatives, we would expect to see at least one of these taxa discussed in all textbooks. At least one of the two taxa did appear in all books: fruit flies appeared in all four textbooks, and beetles appeared in three of the four. However, we found that although beetles, fruit flies and flies were strongly and frequently associated with expanded examples in the literature, they were used primarily for classic examples in the textbooks. In the literature, butterflies and moths exemplified expanded sexual selection, specifically focused on female chemical signals; the books did not attend to these taxa or this topic. What did textbooks use fruit flies and beetles to exemplify? Fruit flies exemplified both classic concepts and one expanded sexual selection concept (sexual conflict) in all books. However, beetles were used only to exemplify classic sexual selection. Thus, although studies of expanded concepts in beetles are available in the literature, they are not typically used to exemplify these concepts in the textbooks.

A similar mismatch is found among the grasshoppers/crickets. Grasshoppers/crickets were often used to study expanded concepts in the literature and also occurred in all four textbooks (Tables 4 ,  5 ). However, the textbooks used them to exemplify mainly classic sex roles. Female-female interactions, signals, and aggression were prominent concepts among grasshoppers and crickets in the literature. Yet in textbooks, the expanded roles received only brief coverage—one, scent marking of males by females, was only listed in a table rather than as a detailed example in the text of the chapter. Another text used a cricket as an example of a flexible sex role, but this appeared only in the end-of-chapter questions.

The significance of our findings, in comparison to most current literature on textbooks, is that we have examined how textbooks track trends in the sexual selection research literature, responding to critiques of gendered and androcentric bias dating back to Darwin’s original writings about sexual selection (Hamlin 2015 ; Jackson 2001a ,  b ,  2014 ). Although we previously found that some textbooks acknowledge the importance of the critique of gendered and androcentric bias in their discussion of sexual selection research (Fuselier et al. 2016 ), their selected images reinforce a traditional view of classic sexual selection theory (Fuselier et al. 2018 ). In this study we find that they also do not engage with its implications when they present the content of sexual selection to their student audience.

Our work concerns the decision-making processes that affect the presentation of knowledge, using the textbooks as a case study and CCE as a framework. Key to this approach is our main finding that in general, the textbooks do not provide a thorough representation of how research in the field of evolution, specifically in sexual selection, has shifted. Our analysis of 1634 unique research papers on sexual selection in insect taxa revealed that although most studies produced work that aligned with the classic paradigm, there were many examples that expanded upon this paradigm; polyandry and other concepts related to female multiple matings were common, as was male mate choice. Additionally, relative to the textbooks, the peer-reviewed research literature reported a greater number of alternatives to classic sex roles occurring in more and different taxa.

Several insect taxa that were included in the textbooks have been used to study alternative concepts; however, instead of reflecting this diversity, the textbooks used those taxa to illustrate classic concepts of sexual selection and excluded the expanded concepts. Thus, we see more attention being paid to alternatives to classic concepts in research articles than in textbooks. One reason for this discrepancy might be due to the taxa that are used to exemplify the concepts. We found some support for this idea in that some taxa in which the alternatives were most frequently studied were not included in textbooks. But this is not the full story because even when textbook authors included taxa that were most strongly associated with alternative concepts, they still focused on the classic concepts instead of addressing the alternatives. This indicates that textbooks maintain a bias toward classic concepts over those that expand the understanding of sexual selection beyond stereotypical sex roles. For example, in the research literature on insect sexual selection, female remating is a common concept, and ‘remating’ has an association with ‘female’ that is even stronger than the association of ‘female’ with ‘choice.’ However, well-studied charismatic insects that would illustrate the benefits of mating multiply for females are not included in textbooks. One example is the honeybee ( Apis mellifera ), a species in which a queen mates with twelve males on average (Tarpy et al. 2004 ); experimental data showed that queens with more than one mate are more attractive to workers, which may give queens longer tenure and thus higher success (Richard et al. 2007 ).

This is significant in the context of research indicating that reading passages in textbooks that reinforce biological bases of difference, whether about humans or not, can lead to more student endorsement of a biological basis behind racial and gendered stratification in society (Donovan et al. 2019b ; Stuhlsatz et al. 2020 ). Thus, there is a critical need to expose students to the kinds of examples about variation in sexual behavior that we found in our review of the research literature on insects in sexual selection, whether through examples provided in the textbooks or in supplementary material to the textbook provided by the instructors. The provision of supplementary materials also offers the chance to engage directly with NOS principles, using the textbooks themselves as the place where scientific knowledge is being constructed. Our work is significant because our case study provides an example instructors can use to address this gap within the framework provided by CCE.

Recommendations for evolution education

Our recommendations align with those made by (Willinsky 2020 ). He found mixed messages both challenging and supporting genetic essentialism in a review of textbook content related to genetics and race. As a teaching strategy, he suggests that instructors directly discuss the variation in how textbooks discuss race and genetics, using this to exemplify the complexity of studying racialized biological outcomes within the historical racist context of science. We concur with his suggestion and position our work as a method to allow instructors to engage more critically with textbook content by exploring with students the social/rational process of scientific work—which necessitates a deeper dive into the formation of the research literature than is present in many textbook summations of scientific content. Our study provides strategies to strengthen the epistemological understandings that students need to ground a robust conception of NOS, by considering the communal, rather than individual, nature of knowledge construction (CCE) in the area of sex and gender difference—an area in which students, indeed all of us, are being bombarded with controversial information.

Students with a more robust understanding of the NOS, especially around the complexities of theory building and testing, understand that knowledge production involves gray areas of nuance and context (Cho et al. 2011 ). To use our work to encourage students to do this, an instructor could ask students to reflect on their views of textbooks. Rather than seeing them as all-knowing repositories that cannot be questioned, such a conversation would encourage what Bazzul ( 2014 ) describes as a reflexive process whereby students engage in ownership of the content of their fields by questioning and considering the nuances of information received. The point of this exercise is not to reinforce a simplistic understanding of the history of racism and sexism in science as a case of bias now corrected, but to have the students use the textbook as a place to think about how information is selected and shaped.

In this instance, our study would provide a strategy to consider knowledge production at the level of the community, with the community at play being the group of evolutionary biology texts, rather than any one individual book. The textbooks that we examined collectively provided coverage of insects that was more representative of the scientific literature than any individual book did. Although there was no single book whose examples of evolution in insects matched the diversity of insect taxa found in the literature, when the books were combined, their coverage came much closer to that diversity.

The use of multiple texts and resources (instead of reliance on one textbook as an authoritative source) has been used in several fields to improve students’ understanding. For example, in history, multiple texts have been used to guide college students to understand the importance of the availability of source material, which can for example be used to indicate which groups have been deemed worth preserving in the historical record and the accompanying writing of history; however, the researchers note that students require training to understand this, given that high school classes present history as a collection of facts to be memorized (Hynd 1999 ). In political science, researchers have identified a hidden curriculum within introductory textbooks that centers institutions and those who have the most power within them (mostly white men), and de-emphasizes or ignores the political contributions of those who have had to fight for equity by segregating coverage of movements for gender, sexual, and racial/ethnic equity into sections linked only to diversity and thus reinforcing the notion that those issues are outside the mainstream (Atchison 2017 ; Cassese and Bos 2013 ); the use of original source material and/or diverse sources from the field’s research literature could ameliorate this bias. Within mathematics, there has been a shift in the conception of how teachers use textbooks, with a new emphasis on teachers’ pedagogical design capacity or the ability of teachers to make decisions about how to use, adapt or add to content provided in textbooks grounded in their understanding of how to help their students learn (Matić, 2019 ). Overall, across a broad range of fields, there is growing recognition that students do not simply receive knowledge from textbooks, teachers or any other source; rather students integrate what they learn with their own frameworks, prior knowledge and goals. Projects that expose for students how textbook authors make choices in their presentation of topics thus offer a way to engage with student sense-making processes and enhance learning (Sikorski and Hammer 2017 ). Comparison across textbooks—making visible their differences as well and what they share—provides a strategy to address this.

Our finding that collectively the books did a better job than any one book in coverage of the field is key here. Instructors could share with their students how their specific class textbook covers topics in contrast to other books. This could lead to conversations about the selection of what to include and not to include and what mediates those decisions, including the authors’ positionalities—not just their identity put a multitude of associated factors based on how they move through the social world—of those doing the research or writing the books—an issue identified as critical to the construction of science by feminist scholars (reviewed in Intemann 2010 ).

Key to this conversation would be including how some of the textbooks’ authors offer overviews of the critique of androcentrism in their fields, framed by noting how those historically excluded from the research community—in the case of gender bias, normally women—corrected this bias by attending to the behavior of female animals (Fuselier et al. 2016 ). Although the discussion indicates the authors saw the value of the critique, it fails to account for the continuing emphasis on classic sexual selection theory, with its androcentric focus and gender binaries. This parallels the split presentation that other researchers found within textbooks—with mixed messaging about race, sex and gender—deconstructing bias in one place, while sharing examples that reinforce it in another passage (Bickford 2022 ; Donovan 2015 ; Willinsky 2020 ). A CCE framework opens the door for a nuanced conversation with students for the reasons behind this finding.

Bringing attention to the increased attention to female behaviors in the context of a discussion of historical and contemporary critiques of sexual selection models for androcentrism would provide a concrete example of the NOS principle that “Scientific knowledge is open to revision in light of new evidence.” This could be accomplished in part by making small shifts in the framing of some concepts and by augmenting textbook examples with examples from different taxa, such as more coleopterans, to represent a wider variety of concepts. In the research literature, Coleoptera and Drosophila were closely associated with concepts related to sperm competition and conflict (sperm competition, male costs, sperm storage, conflict, polyandry, multiple female mating), which require multiple matings among females. Reframing the presentation of sperm competition in textbooks to emphasize multiple mating by females—and the often-positive fitness consequences for females of multiple matings –would put textbooks in closer alignment with the research in this field. Having open discussions with students on the implications of centering sperm competition versus multiple mating or remating by females offers a chance to engage with the NOS principle that ‘Science is a way of knowing’ by having a discussion about the impacts of language choice on who is perceived as having or lacking agency in scientific research.

Further, some taxa used to exemplify classic sex roles, could also be used to show alternatives. A good example would be an orthopteran such as a katydid species that has flexible, condition-dependent sex roles. Although crickets, which are also orthopterans, were used in all textbooks, they were leveraged primarily to support classic sex roles. Again, a small change—adopting examples of orthopteran flexible sex roles in the main body of the chapter—would better align the books with the experimental science. In fact, research on multiple mating by females in orthopterans began in the nineties (Tregenza and Wedell 1998 ). In addition, a class discussion about the reasons why textbooks continue to center classic sex roles could engage students with the NOS principle that “Science is a human endeavor” and is thus subject to the decisions made by humans in terms of what to emphasize, de-emphasize or not to discuss.

Using ACA to track the progress of fields and how they are synthesized in textbooks

For researchers interested in extending this approach to other topics within and beyond sexual selection, we found that ACA is a promising tool for exploring how textbooks reflect the research being done in a particular field, especially which the field is undergoing change in how it approaches key concepts. Our work builds on prior attempts to assess textbook quality by comparing textbooks to the coverage of disciplinary research. For example, Bierema et al. ( 2017 ) used a combination of manual and automated content analysis to identify main topics covered in animal behavior textbooks. For automated analysis, these authors used a program that found terms in text. The difference between this and Leximancer is that Leximancer “learns” from the text and creates a thesaurus of related terms for a particular code. The investigator can then cull the inappropriate terms and ultimately “train” the program to match content with context. This is instructive because it permits researchers to see the relationships among terms and the “composition” of those terms, and then use measures of conditional probability and network analysis to quantify and visualize relationships.

The analysis by Bierema et al. ( 2017 ) determined the proportion of research articles’ abstracts that included four different central ideas in the field of animal behavior. That study used the frequency of occurrence of central ideas in this selection of journal articles, and then compared this to journal impact factor to estimate impact in the field. When they compared these results to textbooks, they found that the textbooks overall matched the literature from 28 journals in that there were similar patterns of proportions across the main topics covered. Using ACA allowed us to conduct a more detailed analysis that provided insights into the relationships among concepts. Also, our research question about taxa was specific enough that we could limit the dataset by taxa rather than by journal; this permitted a broader survey of many journals as opposed to choosing only a selection based on readership or other metrics. Instead of assessing which broad disciplinary topics are covered, we emphasize a focal area within evolutionary biology: sexual selection and the evolution of sex roles and reproductive behavior. This level of detail and nuance was significant for our topic because of our focus on a topic that arose from a critique of mainstream research. Further studies which were outside of the classic view of sexual selection appeared in taxon specific or subfield oriented journals decades before studies were published in mainstream journals (Jackson 2001a , b , 2014 ). Thus, our approach to using ACA is, therefore, appropriate when looking for emergent trends that may counter dominant narratives.

A cautionary note

There are important cautions to bear in mind for those wishing to apply the method of auto-content analysis. One of the biggest challenges is the optimization of search terms to ensure an accurate match between the concept-of-interest and the context in which it is used in the publication. For example, in this study, "multiple female matings" was used more often than “polyandry,” and thus the two terms had to be linked in the thesaurus we created. But then sentences containing the words “multiple,” “female,” and “mating” were considered to be “hits” even when the context of the sentence was not about polyandry (e.g., “…males mating with multiple females…”). Thus, validation, i.e. assessment to determine whether the program is correctly linking the concept to its appropriate context, is critical for an accurate analysis. Human knowledge is required for validation. In our case, the researchers have doctoral degrees in evolutionary biology, animal behavior and gender studies—a diverse group with deep knowledge of the scientific content, including its relation to social movements for gender equality. Additionally, we paid careful attention to the construction of the database, focusing on a collection of papers with a taxonomic focus and manually verifying that the included papers matched our criteria. The technique should be used in conjunction with other methodologies, including thematic coding of text and image analysis, as we have done in other publications (Fuselier et al. 2016 ; 2018 ).

We advocate for the textbooks in a novel way to integrate students understanding of NOS within the context of their study of content. Rather than presenting the textbook as an authoritative source of information, we suggest guiding students through a process of comparing it with the relevant research literature to understand decision making about what aspects of evolution are presented as ‘fact’ to students. This engages students with several tasks shown to be beneficial to the understanding of evolution—metacognitive vigilance (González Galli et al. 2020 ), appreciation of the Nature of Science, especially the tentative and provisional nature of science and the importance of multiple theories, understanding of epistemological beliefs–specifically that learning is changeable, not innate, and knowledge does not come from all-knowing sources– which provide the foundation for a robust understanding of both NOS and evolution (Cho et al. 2011 ).

Availability of data and materials

Data are available by request from the authors.

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Thanks to Briea St. Clair, Rayna Momen, Rachel Stoiko and Sarah Spaulding for their contributions to database construction and prior analyses.

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Jackson, J.K., Fuselier, L. & Eason, P. Automated content analysis as a tool to compare content in sexual selection research with examples of sexual selection in evolutionary biology textbooks: implications for teaching the nature of science. Evo Edu Outreach 17 , 3 (2024). https://doi.org/10.1186/s12052-024-00198-w

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Adaptive evolution: evaluating empirical support for theoretical predictions

Adaptive evolution is shaped by the interaction of population genetics, natural selection and underlying network and biochemical constraints. Variation created by mutation, the raw material for evolutionary change, is translated into phenotypes by flux through metabolic pathways and by the topography and dynamics of molecular networks. Finally, the retention of genetic variation and the efficacy of selection depend on population genetics and demographic history. Emergent high-throughput experimental methods and sequencing technologies allow us to gather more evidence and to move beyond the theory in different systems and populations. Here we review the extent to which recent evidence supports long-established theoretical principles of adaptation.

Introduction

The emergence of adaptive alleles has fascinated evolutionary biologists for decades, inspiring the development of three broad, unifying concepts that underlie adaptive evolution. First, an allele’s probability of fixation depends on the effective population size ( Ne ) of the population in which it arises. Large populations experience more mutations than small ones and thus harbor more potentially adaptive alleles. Furthermore, advantageous segregating alleles are less likely to be lost by random genetic drift in large populations and are more likely eventually to become fixed.

Second, an adaptive allele’s fate depends on its frequency when positive selection begins to act. For de novo mutations, initial frequencies ( p 0 ) are very low, and alleles are likely to be lost by chance, even when they are favored by selection. By contrast, neutral or mildly deleterious alleles may drift to intermediate frequency before becoming advantageous. Such intermediate frequency alleles are less likely to be eliminated by drift and more likely to be fixed by selection.

Third, the magnitude of an allele’s beneficial effect determines how efficiently selection can act to increase its frequency. An allele’s selection coefficient is positively related to its level of control over advantageous traits but is negatively related to possible deleterious pleiotropic effects. These emergent effects of a gene are partially underlain by molecular and biochemical phenomena such as epistatic interactions, linkage to other alleles and gene network position.

Together, Ne , p 0 and selection coefficients provide a foundation for understanding the fate of adaptive alleles ( Fig. 1 ), but modern evolutionary biology requires more detailed and nuanced descriptions of these principles. In some systems, our relatively advanced understanding of biochemistry and molecular biology allows us to explore in depth the functional mechanisms that determine the phenotypic and fitness effects of a mutation. In addition, the emergence of adaptive alleles depends on evolutionary as well as cellular constraints.

The interaction of the selective coefficient ( s ), effective population size ( N e) and initial frequency ( p 0) determines the probability of fixation of an adaptive allele. The x axis is log-transformed for clarity. Homo sapiens 10 , Arabidopsis thaliana 14 and Caenorhabditis elegans 117 all have small historical N e values (of ~10,000), and the probability of fixing a strongly adaptive allele is much lower than for populations with a high N e (such as Drosophila melanogaster 118 and Escherichia coli 119 , which have N e values of 1.1 million and 25 million, respectively). Higher initial frequency increases the chances of fixation of adaptive alleles 45 .

Advances in empirical methods have made possible the study and interpretation of genomic signals of adaptive evolution in different populations and systems. Here we review recent work that highlights the interplay of factors that constrain the emergence and maintenance of adaptive alleles. Moving beyond the theory of adaptive evolution, we discuss how adaptations can arise, what biochemical and physiological constraints they encounter, the nature of the genetic architecture and how the population context of alleles may determine their fate.

Some important disclaimers are required. Natural selection is not the only force that changes allele frequencies; other evolutionary forces include genetic drift, mutation, migration and biased gene conversion 1 . These non-selective processes influence many complex features of organisms. For instance, the assembly of genetic networks through gene duplication and subfunctionalization may be substantially influenced by neutral forces 2 . Also, most of the examples presented here have not explicitly tested the effect of genes or mutations on fitness (but see Ref. 3 for a discussion of this topic). We have chosen examples of phenotypes that plausibly increase fitness in nature, although in most cases the agents and mechanisms of selection were not investigated. We also highlight examples with experimentally imposed selection that avoid this pitfall but that have limitations of their own (reviewed in Ref. 4 ). In addition, we also consider cases in which factors such as deleterious standing variation, genetic drift, mutation pressure and migration influence the fate of alleles.

The impact of population size

Population size and adaptation: the theory.

The probability that any adaptive allele will eventually become fixed or lost depends on the demography of the population in which it arises. One indicator of demographic influences is N e (Ref. 5 ), which can be influenced by factors such as sex ratio, variation in offspring number, inbreeding, mode of inheritance, age structure, changes in population size, spatial structure and genetic structure (reviewed in Ref. 6 ). In humans and other species with expanding populations, very large samples (consisting of >10,000 individuals) are needed to identify the rare, young polymorphisms that reflect current N e values and that may contribute to disease or adaptation from new mutations 7 – 9 . Smaller studies (involving hundreds of individuals) sample older, more common polymorphisms, reflecting historical N e values. Such standing variation may contribute to soft sweeps.

Populations with large N e values are likely to fix adaptive alleles regardless of how strongly they are favored ( Fig. 1 ). They also encounter many mutations each generation6 and therefore have shorter waiting times for adaptive alleles to arise. Small populations, by contrast, sample far fewer mutations per generation and lose many favorable alleles to drift, even those with large selective advantages.

Evidence for population size effects

Despite abundant information on human genetics, we have only begun to understand how our recent evolutionary history influences the emergence of adaptive alleles. Consistent with our small historical N e of ~10,000 (Ref. 10 ), there are few clear examples of new alleles that have spread rapidly to fixation in human populations (reviewed in Ref. 11 ). Instead, recent population expansion has increased human N e (to ~1.1 million in Europe) 9 , resulting in many rare variants that contribute to complex trait variation and disease 7 , 12 .

Comparison of species with different N e values finds that orthologous proteins are less constrained in species with lower N e (Ref. 13 ). Arabidopsis thaliana also has a small historical N e and harbours excess rare and potentially deleterious mutations 14 . By contrast, Drosophila melanogaster has a large N e and appears to gain adaptive alleles frequently from new mutations 15 . The efficacy of selection was measured on three species of mice with similar ecologies but very different N e values 16 . As expected, the species with the highest historical N e had the most adaptive evolution and the most purifying selection 16 . Similar effects of N e have been found in two subspecies of rabbits 17 . However, in two species of Drosophila , higher N e values did not correlate with estimated adaptive evolution 18 , emphasizing that other factors also have an impact on adaptive evolutionary change.

Where do adaptive alleles come from?

Predictions of origins and initial frequency.

An allele favoured by natural selection may be either a new mutation 19 or a pre-existing, segregating genetic variant. If adaptation primarily depends on new mutations, then adaptive change may be limited by the time needed for new mutations to arise and by their stochastic loss. New recessive mutations are primarily found in heterozygotes and are therefore invisible to natural selection until they drift to a higher frequency, when recessive homozygotes become more frequent. In sexual diploids, this bias against the establishment of beneficial recessive mutations is known as Haldane’s sieve 20 . This bias is less important in inbreeding species, in which recessive homozygotes occur more frequently 21 . However, experimental studies to date have not found consistent patterns in the degree of dominance for new mutations (reviewed in Ref. 22 ).

Alternatively, a pre-existing neutral allele can drift to intermediate frequency and can later become advantageous when selection pressures change owing to environmental change or to colonization of a new habitat. Alleles from standing variation have several advantages over new mutations. First, populations do not have to wait for new mutations to arise because the alleles are already present. Second, the allele may be at a higher frequency, decreasing the probability of loss by drift ( Fig. 1 ). This is especially true for beneficial recessive mutations, as dominance has little influence on the fixation of alleles from standing variation, but it is very important for new mutations or very low frequency alleles 23 . Such pre-existing alleles may have already recombined onto several genetic backgrounds, which also ‘hitchhike’ to a higher frequency with the favored allele 19 in a process known as a soft sweep ( Box 1 ).

Inferences about adaptive evolution from sequence data: Caveats

Adaptive alleles may be derived from new mutations or from pre-existing standing variation. In a classic (hard) selective sweep, new mutations appear on a single haplotype that quickly goes to fixation. Therefore, when the genome is scanned after a hard sweep, a pattern of reduced nucleotide variation may be found near the adaptive mutation. By contrast, in soft sweeps, favored variants occur on multiple genetic backgrounds (haplotypes), and the variation among haplotypes obscures the reduction in polymorphism around favored variants 111 , making soft sweeps difficult to detect. Such soft sweeps can occur if old, standing genetic variation has recombined onto several genetic backgrounds before it becomes advantageous or if independent advantageous mutations occur in parallel. Finally, signatures of selective sweeps may be obscured by population structure, and variation may resemble selection on standing variation 112 . Indeed, identifying soft selective sweeps has been one of the most challenging problems in molecular population genetics. However, a recent analysis of changes in allele frequency at height-associated polymorphisms finds clear evidence for selection on pre-existing polygenic variants — an analytical approach that should be broadly applicable 38 .

Several population characteristics influence the probability of a hard versus a soft sweep. Soft sweeps are more likely when populations are large or when mutation rates are high 113 , whereas small populations or low mutation rates favorr hard sweeps from a single, new mutation. In addition, soft sweeps are more likely in widely distributed species with low migration rates 27 , facilitating parallel sweeps in different parts of a species range.

Epistasis and rejecting neutrality

Many tests for selection use evidence of fixation of multiple adaptive mutations. For example, the McDonald–Kreitman test 114 examines polymorphism and interspecific divergence at multiple sites to detect natural selection. However, epistasis among sites in a protein may cause false rejection of the null hypothesis of neutral evolution 115 . Instead, a locus with an extreme McDonald–Kreitman statistic might actually reflect a neutral permissive mutation that changed protein functional constraints and that enabled subsequent neutral mutations to occur. Thus, given the demonstrated importance of epistasis within proteins 84 , 85 , inferences of adaptive evolution made from the McDonald–Kreitman tests must be made with caution.

Adaptive change does not necessarily require fixation of advantageous alleles. Instead, modest changes in allele frequencies at many loci can increase population fitness 11 . The raw material for polygenic adaptation may come from standing variation, and slight changes in gene frequencies support the fine-tuning of a trait to a new or changing environment 24 .

Does theory predict whether adaptive alleles are more likely to arise from new mutations, fixation of standing variation or modest changes at many loci? The answer lies in the effect size of the mutation on fitness 25 , which is influenced by gene network position, linkage to other loci and epistatic interactions, as discussed in the section below.

Evidence for adaptive alleles arising from new mutations

Because large populations sample more new mutations and can efficiently select for weakly favored alleles, they should respond to natural selection more readily than small populations. In D. melanogaster , which has a very high N e, several adaptations have been attributed to new mutations 15 , 26 . In one striking example, convergent insecticide resistance arose in isolated D. melanogaster populations several times in the past 50 years 15 . Many insecticides target a neuronal signalling enzyme encoded by the Acetylcholine esterase ( Ace ) locus, and four sites in Ace have mutated to cause insecticide resistance in different local genetic backgrounds. In non-selective environments, the derived mutations are deleterious, but they confer a strong advantage in the presence of insecticide. The haplotype structure and deleterious effects under non-selective conditions rule out the possibility that these mutations arose from standing genetic variation (but see Box 1 ). This example demonstrates local hard sweeps for insecticide resistance, and a soft sweep with parallel changes at the species scale, as predicted by theory 27 . These results suggest that under strong selection, D. melanogaster can quickly sample and fix new adaptive alleles in response to selective pressure. These results are consistent with genome-wide studies of polymorphisms 28 that find lower variation around amino acid substitutions than around synonymous substitutions, suggesting that selective sweeps are common in D. melanogaster .

Evidence for adaptive alleles arising from pre-existing variants

Adaptations arising from standing variation may be at moderate frequency when they become advantageous. Many well-characterized adaptive alleles arose from standing variation 29 – 31 . For instance, light coloration in beach mice has a single origin that has probably been selected from standing variation in melanocortin 1 receptor ( Mc1r ) in mainland populations 32 . Similarly, an allele for reduced plate armor in sticklebacks segregates in the source ocean population and has gone to fixation independently in several freshwater colonizations 30 , 33 . Several other examples (reviewed in Ref. 11 ) have shown that standing variation facilitates fast adaptive responses to strong selection.

Although the fixation of alleles is clearly important to adaptation, it is not required for large changes in phenotype 11 , which may result from slight changes in allele frequency at many loci. Such changes are usually difficult to detect, yet several directed evolution studies in D. melanogaster 34 , 35 support this model of adaptation by polygenic allele frequency changes. Human populations that span a wide range of geographic locations and climates also appear to have evolved in this manner 36 – 38 .

Because soft sweeps have been difficult to detect in natural populations ( Box 1 ), empirical studies have so far struggled to infer their importance relative to hard sweeps. Patterns of nucleotide polymorphism support a role for hard sweeps in wild D. melanogaster populations 26 , but a long-term selection experiment for accelerated development suggested soft or incomplete selective sweeps 34 . Few examples of hard sweeps have been found in genome-wide studies of species with a small historical N e (namely, humans and Arabidopsis thaliana 14 , 39 ), although soft sweeps at multiple loci influencing human height have been inferred in European populations 38 . Thus, some combination of soft sweeps and poly-genic allele frequency changes may influence adaptive variation of complex traits.

Adaptation by introgression from other species

Introgression from closely related species appears to be an important but underappreciated source of new adaptive alleles. For example, dark coloration arose through artificial selection in domestic dogs by means of a mutation in Mc1r . This allele introgressed into wolves and rose in frequency in the boreal forest but not in tundra habitats, where the ancestral grey color is putatively advantageous 40 . Introgression between domesticated species and their wild relatives is an intriguing source of new alleles, because humans can maintain breeding populations of domesticated species that carry mutations that would be disfavored in wild populations. The exchange of color pattern mimicry genes by congeneric Heliconius butterflies 41 shows that natural selection can facilitate adaptive evolution by introgression. Similarly, a human leukocyte antigen (HLA) class I allele originating in archaic humans introgressed into modern Asian populations 42 . This allele spread and later introgressed back into African populations, suggesting that an important contributor to immune defense in modern humans arose through admixture.

Strength of selection

Theoretical models of effect size.

Genes vary in their level of control over phenotypes, and the evolutionary fate of new mutations depends on their effect size on selectively important traits. Two contrasting models represent extremes along a continuum of effect sizes. Under the polygenic or infinitesimal model, trait variation is controlled by many loci with small effects 24 . As the number of loci controlling a phenotype increases, their individual effects tend to decrease, and the average strength of selection on any locus is reduced 5 . Consequently, most beneficial mutations have a high probability of being lost, even in large populations, because their selective coefficients are small 5 .

Alternatively, some adaptive alleles can be classified as major genes 43 . Because advantageous major alleles are theoretically much rarer than small-effect alleles 44 but are also less susceptible to loss by genetic drift 45 , intermediate-size mutations are likely to be over-represented during adaptive evolution. Under some circumstances, this may result in an exponential distribution of effect sizes, with a few major and many minor genes contributing to adaptation 43 , 46 . Major-effect mutations include many unconditionally deleterious alleles (for example, Mendelian diseases) as well as variants with environment-specific fitness (for example, see Ref. 29 ), which might become adaptive when environments change.

Observations of effect size

Genomic analyses reveal a broad diversity of genetic architectures, including many small-effect genes, major genes and mixtures of polygenic and Mendelian determinants of trait variation. Human height exemplifies many of these patterns. At least 180 loci control variation within and among populations and together explain ~10% of phenotypic variation in height. Meta-analysis 47 finds that some small-effect genes controlling human height also have pleiotropic influences on other traits, especially physiological components related to type 2 diabetes risk. For height and many other traits, intermediate frequency alleles have small phenotypic effects, whereas rare alleles may have larger effects on traits 7 , 9 , 12 ( Fig. 2 ).

Findings from a meta-analysis illustrate the population frequency of the rarer allele on the horizontal axis versus the effect size of that allele on the vertical axis. Colors indicate levels of statistical significance for the association of alleles with the trait. Results show that large effect alleles are fairly rare for this heritable, selectively important trait 47 . Figure reproduced, with permission, from Ref. 47 © (2011) Cell Press.

Large studies of some traits support both the infinitesimal and major gene models. In D. melanogaster , strong artificial selection has resulted in large changes in SNP frequencies with the involvement of mostly small-effect loci 34 , 35 , although some field experiments have found evidence of large-effect quantitative trait loci (QTLs) 48 . In general, most individuals express polygenic variation, whereas phenotypically extreme individuals may reflect non-additive gene action or rare, large-effect alleles 49 . These extremes may involve additional loci and pathways contributing to human disease and can be very valuable for breeding domesticated species 50 . Surprisingly, genes that contribute to both Mendelian and complex diseases in humans 51 show different molecular and network properties compared to loci controlling only Mendelian or only complex diseases; specifically, genes that control both complex and Mendelian diseases are longer, more highly transcribed, more tissue-specific in their expression and are embedded in more complex protein networks. The discovery of patterns in these genes is an important step towards predictive approaches to complex trait variation.

Networks and effect size: theory

The position of a gene product in its biochemical or regulatory network influences its effect size. Theory predicts that the first enzyme in a metabolic pathway will have more influence on the total output of a pathway than downstream enzymes 52 , 53 (but see Ref. 54 ). The same principle should apply to perception signal transduction pathways, in which the genes that directly interact with environmental stimuli, pathogen effectors or pheromones are upstream of all other genes that modulate responses to those exogenous signals. Similarly, a highly connected transcription factor ( Fig. 3 , nodes A and E) that integrates or directs expression of many genes is predicted to have stronger phenotypic effects than a peripheral regulator that influences only a few relevant genes 55 ( Fig. 3 , node F). Finally, even a gene with low connectivity can have a large effect if it has high centrality 56 ( Fig. 3 , node D).

A gene’s position in a regulatory network influences its effects on a target phenotype and on other traits. Circular node sizes are proportional to the gene’s effect on the selected phenotype; the intensity of red coloration is proportional to effects on other traits (where no color indicates no effect on other traits). Square nodes have no effect on the target phenotype owing to the directionality of the network, but they may influence other phenotypes. Small black circles indicate the directions of the interactions in the network; modes of interaction are not specified. Genes encoding upstream proteins (A) often have large effects because they control many downstream genes influencing a trait, although pleiotropy mediated by other connections may weaken net selection on these ‘hub’ genes. Compared with protein A, the gene encoding protein B has fewer pleiotropic connections but also less control over the target phenotype. Protein C has lower pleiotropic constraint than protein B and integrates more upstream signals — including environmental inputs — resulting in higher evolvability. Proteins at central or ‘bottleneck’ positions (D) often have large effects, even if they have few direct connections with other proteins. Proteins with both high centrality and high connectivity (E) may be influenced by large-effect, adaptive alleles. Genes encoding downstream, peripheral proteins (F1 and F2) may have small to moderate effects and are more likely to accumulate neutral or nearly neutral variants than relatively upstream genes of large effect (D and E), which may evolve under positive and then purifying selection.

Pleiotropic effects may change the net advantage of an allele. Which loci tend to affect multiple phenotypes? Crosstalk between biochemical pathways results from the partitioning of precursors and intermediates, such as when an enzyme’s product is a substrate for multiple downstream enzymes 57 . Similarly, transcription factors with high connectivity to multiple gene networks affect more traits than those with only a few target genes 55 ( Fig. 3 , nodes A and B).

Because natural selection works more efficiently on loci that exert large effects on phenotypes, the evolution of such loci is more likely to be constrained by purifying selection 58 . Most new mutations will quickly be purged from these loci, which will therefore accumulate little genetic diversity. By contrast, other loci may tolerate more mutational changes and may accumulate genetic variants that could become adaptive after a change in environment or genetic background 59 . The trade-off between strong positive selection and purifying selection has been demonstrated by simulated evolution of both biochemical 53 and regulatory networks 55 ( Box 2 ).

Comparing biochemical and regulatory networks

How different are the evolutionary consequences of position in metabolic versus regulatory networks? The two network types reflect very different biological processes: biochemical pathways consist of a series of enzymes modifying chemical substrates, whereas regulatory networks may involve phosphorylation changes or soluble proteins binding to DNA. Nevertheless, they share analogous features that have important consequences for adaptive evolution.

For example, the phenotype produced by a linear metabolic pathway is the concentration of final chemical product, and for a linear regulatory cascade it is the concentration of final gene product. Genes included in more than one such pathway can influence multiple phenotypes. If a biochemical intermediate is generated faster than the next enzyme can process it, it will remain in solution or be diverted to compatible enzymes in other pathways, thus altering non-target phenotypes and creating possibly toxic intermediates 57 . Similarly, if the concentration of a transcription factor is higher than can simultaneously bind to a target gene, it may bind to alternative targets 116 . Finally, in much the same way as enzymes can evolve different substrate affinities and catalytic rates, transcription factors have evolvable affinities for DNA sequence motifs. In both cases, the interaction between two genes can be affected by mutations in either locus.

Recent simulations of regulatory and metabolic pathway evolution have identified similar patterns. A regulatory network adapting to ecological challenges in silico quickly developed a hierarchical structure dominated by a few global regulators 55 . Notably, these patterns were not observed in parallel simulations of regulatory network evolution under neutral conditions 55 . The analogous simulation of metabolic pathway evolution found that upstream enzymes tend to have the most control over phenotype and also be the target of natural selection 53 . In both cases, large-effect genes in upstream parts of the protein networks evolved under strong positive selection and then became constrained by strong purifying selection, after which further evolution of the system proceeded only through neutral or nearly neutral mutations in peripheral genes of small effect.

In conclusion, metabolic and regulatory networks share many of the properties that determine the effect size and pleiotropy of the networked genes. Enzymes and transcription factors with high connectivity — that is, receiving input from many other genes and/or transmitting output to many other genes — are likely to be highly pleiotropic. In general, genes with high centrality — that is, genes at bottlenecks or branch points — are particularly important components of protein networks 56 , 57 .

Networks and effect size: observations

When a molecular network is well-characterized, the evolutionary histories of genes occupying different positions can be compared. This approach was used to investigate selection on human innate immunity against bacterial pathogens 60 . The authors used resequencing data from 132 innate immune system genes to test the effects of network position on evolvability. Their results conform well to theoretical predictions: genes with a high connectivity and/or centrality harbor significantly less nucleotide diversity than genes on the periphery of the network 60 . The genes that are most likely to show signatures of positive or balancing selection are pathogen recognition receptors (the most upstream part of the network) and the downstream functional modules that carry out the immune response. By contrast, the most strongly conserved genes integrate inputs from the numerous pathogen recognition receptors and coordinate the activity of the downstream functional modules 60 . These highly connected, highly centralized global regulators are presumably so essential to the immune response that slightly deleterious mutations are quickly eliminated.

Similar studies of the insulin and target of rapamycin (TOR) pathways, which are instrumental in growth regulation and are highly conserved among eukaryotes 61 , provide an interesting contrast to theoretical expectations and to the immunity case study 60 . Centrally located and highly connected genes in the human insulin and TOR pathways show increased positive selection 62 ; this is the opposite pattern from the human immunity network, in which central genes are under stronger purifying selection and the peripheral genes show positive selection 60 . Furthermore, contrary to theoretical predictions, downstream genes in the insulin and TOR pathways are more constrained than upstream genes in Caenorhabditis spp. 63 , vertebrates 64 and Drosophila spp. 65 . Several hypotheses are invoked to explain these unexpected patterns of selection on insulin and TOR network genes. The tendency of downstream genes to be more constrained than upstream genes was first attributed to a positive correlation between network position and intensity of pleiotropy 65 . Alvarez-Ponce et al . 64 revised this hypothesis to suggest that the pleiotropic effects of downstream genes simply have greater fitness consequences than those of upstream genes. Jovelin and Philips 63 concluded that differential expression level is the best explanati on for stronger purifying selection on downstream insulin and TOR genes. Usually, however, upstream genes show evidence of stronger selection, whether it be purifying 53 , 60 or positive selection 66 – 68 . Notably, selection on genes that interact directly with the environment has been implicated in the evolution of olfactory perception in mammals 69 and light perception in cichlid fishes 70 . Because some examples support predictions from network theory but others consistently defy them, it is clear that our understanding of adaptive gene network evolution is incomplete.

Regulatory variation: circumventing pleiotropic constraint

Deleterious pleiotropic effects may be circumvented by mutations in regulatory elements that allow flexibility in the amount, timing and location of gene expression 71 . For instance, a missense mutation could simultaneously eliminate all functions of a protein, which could have serious pleiotropic consequences. By contrast, a regulatory mutation might alter gene expression only in specific tissues, developmental stages or environmental conditions. The duplication or deletion of regulatory elements could incrementally increase or decrease concentration of a gene product. Thus, the modular nature of gene regulatory sequence may allow a gene to evolve with less pleiotropic constraint 71 .

In practice, adaptive molecular evolution may involve coding mutations in key proteins: for example, tetrodotoxin resistance in garter snakes 72 . Regulatory variants, however, have recently been implicated in the evolution of adaptive traits, such as sex pheromones in moths 73 and resistance to Lassa fever in humans 74 . Notably, mutations in tissue-specific cis -regulatory elements allowed the loss of seed shattering in rice and Brassica spp. 75 and pelvises in sticklebacks 76 ; in both cases, full knockout of the target gene had lethal or clearly deleterious pleiotropic effects.

Epistasis and adaptation

Predicting the effects of epistasis.

To understand how genes influence traits under selection, we must consider how their genetic context influences their selection coefficients. Epistatic interactions are commonly visualized on a theoretical surface known as an adaptive landscape 77 . The shape of an adaptive landscape heavily depends on the extent and nature of epistasis ( Fig. 4 ).

Panels a , b and c illustrate possible transitions from a low-fitness progenitor ( ab ) to a high-fitness derived state ( AB ). Panels d , e and f illustrate mutational trajectories under different epistaticconditions, as predicted in Refs. 67 , 69 . a | When epistasis is absent, a change from a to A or from b to B has identical fitness consequences, regardless of the other locus. b | With negative epistasis, transition from ab to either aB or to Ab gives an identical fitness increase. However, the subsequent mutation to AB further increases fitness by a small amount. Thus, the fitness effect of a to A and of b to B depends on genetic background but changes only in magnitude, not in sign. c | Sign epistasis can cause a change in rank fitness, depending on the genetic background. For example, the a to A transition is deleterious in the b genetic background, but it is advantageous in the B background. d | Without epistasis, there is no relationship between the selective advantage of a mutation and the fitness of the genetic background in which it occurs. e | With negative epistasis, new beneficial mutations confer a smaller fitness increase when they occur in a genetic background with relatively higher fitness. f | With sign epistasis, only very specific mutations in specific genetic backgrounds increase fitness; the same mutations would decrease fitness if they occurred in other genetic backgrounds. Panels a – c are modified, with permission, from Ref. 79 © (2005) Macmillan Publishers Ltd. All rights reserved. Panels e and f are reproduced, with permission, from Ref. 82 © (2011) American Association for the Advancement of Science.

In the absence of epistasis, adaptive alleles are equally advantageous regardless of genetic background ( Fig. 4a ). In this scenario, populations can readily evolve towards a nearby adaptive peak. However, if epistasis is common, the benefit of an adaptive allele depends on pre-existing and subsequent mutations, potentially preventing a population from climbing the nearest fitness peak 78 . Even the type of epistasis may influence the progress towards a local peak. Sign epistasis 79 ( Fig. 4c ) creates a rough fitness landscape in which the chronological order of adaptive substitutions is important, because many mutational pathways contain unfit steps. Evolution to a fitness optimum may be impossible in some genetic backgrounds because all single mutational steps towards the optimum are inaccessible owing to deleterious epistatic interactions ( Fig. 4c ). However, with negative epistasis ( Fig. 4b ), a series of adaptive substitutions can take place in almost any order: the first substitution causes the greatest fitness gain and subsequent changes have diminishing returns. Most theoretical and experimental research in this area has focused on haploids owing to the additional complications that arise with diploidy 80 .

Evidence for the effects of epistasis

When epistatic interactions occur among mutations, the order in which multiple adaptive changes arise may make a large difference. It was noted that the rate of adaptation slows as populations approach an optimum: large-effect changes occur first, and minor changes occur last 81 . This observation could be caused by one of two principles. In one scenario, the first allele to become fixed does so because it has the highest selective advantage regardless of background, and major alleles generally reach fixation more quickly. Alternatively, the selective advantage of any beneficial allele is context-dependent, such that any early-arising allele has larger beneficial effects than any subsequent mutation.

Two independent experimental evolution studies find that epistasis between adaptive alleles shows diminishing returns from late-occurring mutations. In one study, the endogenous Methylobacterium extorquens methanol metabolism pathway was replaced with an engineered pathway and selected for use of methanol as the sole carbon source 82 . Fitness measurements of all combinations of the five beneficial mutations that arose during adaptation showed that four of the five mutations exhibit decelerating fitness gains during adaptation ( Fig. 4f ). The other study investigated the beneficial mutations that arose during a long-term Escherichia coli evolution experiment on glucose-limited media 83 . Again, when all combinations of beneficial mutations were tested, all mutations increased fitness, but smaller selective increments were seen in higher fitness backgrounds. In both of these scenarios, the order of the mutations appears to be irrelevant, as the first mutation gives a large increase in fitness, the second gives a lesser gain, and so on. Thus, in these cases, all mutational trajectories are accessible. The magnitude of the fitness gain caused by an adaptive allele heavily depends on the preceding mutations, but its sign is always positive.

In contrast to the smooth landscape seen for multi-locus adaptation, it was found the landscape of within-protein adaptive alleles is very rough 84 . Only 18 of 120 possible trajectories of beneficial mutations in the E. coli TEM beta-lactamase gene were favored by natural selection ( Fig. 4f ). This pattern also holds for the fitness landscape of isopropylmalate dehydrogenase (IMDH) 84 , in which only 29% of possible mutational trajectories are selectively accessible. Within-protein epistasis is strong, and substantial sign epistasis makes the chronological order of adaptive alleles important. As shown by Fig. 4f , each of the five mutations increases the selective advantage, but their positive effect strongly depends on the background in which they arose. Given the clear importance of sign epistasis in proteins 85 , neutral, permissive mutations probably occur frequently 86 , constantly changing selective coefficients of nearby mutations ( Box 1 ).

Among the well-characterized examples of natural adaptive alleles, epistasis appears to be extremely important. In beach mice, the interaction between MC1R and agouti controls coat colour. The agouti protein determines the expression of MC1R and is a stronger antagonist in light coloured mice, in which MC1R function is impaired 29 . Within-protein epistasis is also responsible for widespread drug resistance in the H1N1 virus 87 . Although they do not provide the same level of mechanistic detail as experimental evolution, these natural examples indicate that epistasis has an important role in natural variation, at least in the large-effect genes that are most easily detected in nature.

Recombination and adaptation

Predictions of the effects of recombination.

Another phenomenon that affects the emergence of adaptive alleles is recombination, which can separate adaptive alleles from linked maladaptive ones and thus can facilitate their fixation 88 ( Fig. 5c ). Tightly linked deleterious sites reduce the net selective coefficients of adaptive alleles. Additionally, alleles can spread among populations more easily when they are in regions of high recombination. Thus, theory predicts that adaptive alleles are more likely to arise in areas of high recombination (reviewed in Ref. 89 ).

a | Consider two ecologically important genes, D and E , segregating for alleles that are adapted to different environments. Alleles D and E are best suited to environment 1, and alleles e and d are best in environment 2. Finally, genes X and Y are neutral loci. Mating between DE and de can produce maladaptive haplotypes De and dE . b | An inversion on the DE haplotype will repress recombination between these loci and increase fitness of these alleles in the ir favored environment. c | If alleles f and g are maladapted, then recombination between them will produce the high fitness FG haplotype. In this case, recombination aids in the emergence of adaptive haplotype FG . d | The inland, annual ecotype of Mimulus guttatus occurs in seasonally dry habitats and flowers early in the spring, whereas the sympatric coastal, perennial form is found in wetter areas and is dormant in the early spring and flowers later. Hybridization between these ecotypes would produce offspring that are less fit in either habitat. Traits that confer local adaptation to these distinct environments are located on an inversion (shown as a long rectangle) that preserves these phenotypic combinations 81 . e | Heliconius butterflies are a classic example of Mullerian mimicry . Many species of the genus Heliconius (for example, Heliconius numata silvana and Heliconius numata aurora ) mimic the wing patterns of Melinae spp. to avoid predators. Each of these wing patterns requires a distinct combination of alleles that influence color and shape, and recombinants between these distinct types are maladapted. The different Heliconius mimics are closely related and occur sympatrically, yet hybrids are rarely found in nature. It has been shown that two phenotypically distinct mimics have an inversion that harbors at least two color-pattern loci 97 . Photographic images in panels d and e were provided by David Lowry (University of Texas at Austin, USA) and Mathieu Joron (Muséum National d’Histoire Naturelle, Paris, France), respectively.

Alternatively, recombination may decrease fitness by separating co-adapted alleles 90 ( Fig. 5a, b ). For example, when populations adapt to different niches, alleles that are advantageous in one environment may be deleterious in another. Decreased recombination between these sets of co-adapted genes reduces the production of offspring that are maladapted to both environments ( Fig. 5a ). Thus, chromosomal inversions containing multiple co-adapted alleles increase fitness because they suppress recombination between divergent types ( Fig. 5b ), resulting in fewer unfit recombinant offspring 91 . In some circumstances, therefore, reduced recombination may be advantageous.

Evidence of the effects of recombination

Generally, recombination is expected to increase the efficacy of selection for adaptive alleles ( Fig. 5c ). For instance, proteins in regions of low recombination suffer from a larger load of deleterious mutations and fewer beneficial mutations compared to those in regions of high recombination 92 . Additional evidence comes from the positive correlation between recombination rate and nucleotide diversity 93 , 94 , which could be generated by background selection or hitchhiking near adaptive alleles. In humans, divergence among populations is negatively correlated with recombination rate 95 , suggesting that alleles in areas of high recombination can spread more easily among populations because they are less constrained by linked deleterious mutations. Although this is only an indirect link between recombination and the emergence of adaptive alleles (and may be confounded by background selection), it is clear that recombination can increase the efficiency of natural selection 90 .

When multiple loci control complex phenotypes, however, recombination may break up groups of co-adapted alleles. Therefore, a non-recombining inversion can function as a single locus, and the collective effects of multiple loci may jointly be favored 96 . Two recent studies 97 , 98 document cases in which sympatric but ecologically distinct ecotypes maintain their respective sets of adaptive alleles on inversions ( Fig. 5d, e ). These examples highlight the importance of inversions for maintaining specific trait combinations in locally adapted, sympatric species. However, several questions remain. How common are adaptive inversions in nature? How do inversions gain adaptive alleles? Does an inversion event prevent the gain of new genes in the future, or can new adaptive alleles be ‘captured’ by an inversion after it has been established?

Models of migration and adaptation

Migration influences the emergence of advantageous alleles in several ways. Gene flow between populations that are locally adapted to divergent environments may increase genetic variability within habitats 99 , some of which may lend itself to adaptation. Indeed, recent theory suggests that high gene flow among locally adapted populations encourages the emergence of fairly large-effect QTLs 100 that may consist of several linked, small-effect loci. However, if the migration from one habitat overwhelms the other, migration from the source could prevent adaptation to marginal habitats 101 . Finally, gene duplicates may be selectively favored when nearby populations experience maladaptive gene flow 102 because duplicated local alleles may be able to mask maladapted immigrant alleles. In particular, tandem duplications can increase in frequency when populations experience immigration of locally deleterious alleles, suggesting that such migration–selection balance would favour increased copy number variation, which is common in many species (for example, see Ref. 103 ).

Migration and adaptation in practice

The prediction that migration–selection balance causes higher levels of genetic variation in environmentally heterogeneous areas is supported by a large study in lodgepole pines, in which regional climatic heterogeneity predicts complex trait variation in common gardens 104 . This positive correlation between environmental and genetic variation suggests that the immigration of deleterious alleles from divergent environments increases local genetic diversity. However, a recent experiment with D. melanogaster in heterogeneous laboratory environments found no evidence that environmental heterogeneity increases genetic variation 105 . Several recent studies of gene flow among plant populations support the prediction that immigration of maladapted alleles may limit the capacity of populations to adapt to local environmental conditions 106 , 107 . Future progress in understanding the role of migration–selection balance and whether environmental heterogeneity can maintain genetic variation will benefit from experimental studies in natural populations 105 , especially for known QTLs experiencing natural selection.

Conclusions and perspective

The integration of evolutionary theory with modern genetics and genomics has yielded deep insights into the emergence of adaptive alleles. Although a full understanding of evolution must also consider non-selective forces 3 , a focus on the process of adaptation is especially valuable in medicine, agriculture and conservation biology, in which the functionality of adaptive changes has direct importance for humans and our environment.

Recent empirical evidence supports some major theoretical predictions but not others. For instance, the implication of both small-effect and large-effect QTLs in genetic adaptation suggests that both the infinitesimal and Mendelian models may be correct 49 , 51 . Similarly, the importance of epistasis 82 , 83 , 87 and recombination 97 , 98 in adaptive evolution is well-supported, and examples of adaptive alleles originating both from new mutations 15 , 26 and standing genetic variation 29 – 32 have been documented.

However, conflicting results prevent resolution of long-standing theoretical debates about the roles of hard and soft selective sweeps 14 , 26 , 39 , and the effect of N e on the efficiency of selection 18 . It is possible that these contradictions are simply due to inherent difficulties in detecting sequence signatures of adaptive evolution ( Box 1 ); the availability of more sequences and improved analytical methods may eventually lead to more conclusive results. Additionally, although some studies validate predictions from molecular network theory 60 , 66 , other examples consistently defy expectations 62 – 65 , indicating that the effects of pathway and network position on adaptive value are more complex than previously thought. More detailed studies of the functional effects of gene product interactions may shed light on these confusing patterns.

This Review has addressed adaptive evolution and how population genetic factors influence the emergence of alleles. Thus, we have not discussed the selective environment itself, which is obviously a major factor shaping the course of adaptive evolution. For example, biotic agents of selection such as mate choice, predators or pathogens are more likely to elicit responses through large-effect QTLs 68 and strong balancing selection than are abiotic selection pressures 108 , 109 . Furthermore, adaptation in complex environments will probably differ from adaptation in simple environments, such as those in laboratory experiments — not only because selection pressures vary with the environment but also because gene effects often interact with environmental stimuli. Alleles that are beneficial in one habitat often have different fitness effects in other environments, and this has important consequences for population variation and evolutionary change.

Our empirical understanding of adaptive evolution has greatly progressed in the past decade, yet many challenges remain. Pathway and network analyses of complex traits 110 offer great potential to elucidate the causes of phenotypic variation and evolutionary change. Apart from agents of selection and gene-by-environment interactions (which are best investigated using a combination of functional genomics, evolutionary genetics and environmental context), many questions about adaptation at the molecular level could be resolved by additional work in the systems reviewed here. Experimental evolution is a particularly promising method for isolating individual factors affecting adaptation and for explicitly testing the interplay among such factors, yet we do not know whether the inferences drawn from such studies can apply to natural systems. Studies of human complex traits and disease have catalyzed a revolution in omics technologies that benefits studies in many organisms, promising additional opportunities to test evolutionary hypotheses.

Acknowledgments

We thank J. T. Anderson, D. Lowry, P. Magwene, A. Schmid and three anonymous reviewers for helpful discussion and comments. We also acknowledge the authors of the many excellent studies that could not be included in this review due to space limitations. This work was supported by the National Institutes of Health (award R01 GM086496 to TM-O; Training Grant 5T32GM007754-32 to Duke University Program in Genetics and Genomics) and the National Science Foundation (award EF-0723447 to TM-O; dissertation grant 1110445 to CO-M).

Biographies

Carrie Olson-Manning received her B.S. in genetics and evolution at the University of Minnesota, USA. Her interest in the genetic and biochemical basis of evolution began while working as an undergraduate in the laboratory of Tony Dean. To pursue her interest in natural variation, Carrie is working towards a Ph.D. with Thomas Mitchell-Olds at Duke University, USA. Her dissertation research focuses on the genetic basis of a plant chemical defense against herbivory and the evolution of biochemical pathways.

Maggie R. Wagner graduated from the University of Michigan, Ann Arbor, USA with a B.S. in plant biology. She became fascinated with the intersection of ecology, microevolution, and phenotypic diversity during a research internship at Harvard Forest, Massachusetts, USA and several years working at the University of Michigan Herbarium. Her Ph.D. research with Thomas Mitchell-Olds at Duke University, North Carolina, USA examines the evolution and genetic basis of reaction norms and genotype-environment interactions in plants under spatially variable herbivory pressure.

Thomas Mitchell-Olds received his Ph.D. from the University of Wisconsin-Madison, USA, and spent one year as an NIH postdoc in human genetics. He is a former Director of the Max-Planck Institute of Chemical Ecology in Jena, Germany. At Duke University he is Professor in the Department of Biology and Institute for Genome Sciences and Policy, and is active in the graduate programs in Biology, Genetics and Genomics, and in Computational Biology and Bioinformatics. His research focuses on the functional basis and evolutionary causes of genetic variation in populations.

The authors declare that they have no competing financial interests.