Sexual Selection Research Research Articles

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

Background 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.ResultsThe 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.

New estimates indicate that males are not larger than females in most mammal species

Sexual size dimorphism has motivated a large body of research on mammalian mating strategies and sexual selection. Despite some contrary evidence, the narrative that larger males are the norm in mammals—upheld since Darwin’s Descent of Man—still dominates today, supported by meta-analyses that use coarse measures of dimorphism and taxonomically-biased sampling. With newly-available datasets and primary sources reporting sex-segregated means and variances in adult body mass, we estimate statistically-determined rates of sexual size dimorphism in mammals, sampling taxa by their species richness at the family level. Our analyses of wild, non-provisioned populations representing >400 species indicate that although males tend to be larger than females when dimorphism occurs, males are not larger in most mammal species, suggesting a need to revisit other assumptions in sexual selection research.

When less is more: coy display behaviours and the temporal dynamics of animal courtship.

Sexual selection research has been dominated by the notion that mate choice selects for the most vigorous displays that best reflect the quality of the courter. However, courtship displays are often temporally structured, containing different elements with varying degrees of intensity and conspicuousness. For example, highly intense movements are often coupled with more subtle components such as static postures or hiding displays. Here, we refer to such subtle display traits as 'coy', as they involve the withholding of information about maximal display capabilities. We examine the role of intensity variation within temporally dynamic displays, and discuss three hypotheses for the evolution of coy courtship behaviours. We first review the threat reduction hypothesis, which points to sexual coercion and sexual autonomy as important facets of sexual selection. We then suggest that variation in display magnitude exploits pre-existing perceptual biases for temporal contrast. Lastly, we propose that information withholding may leverage receivers' predispositions for filling gaps in information-the 'curiosity bias'. Overall, our goal is to draw attention to temporal variation in display magnitude, and to advocate possible scenarios for the evolution of courtship traits that regularly occur below performance maxima. Throughout, we highlight novel directions for empirical and theoretical investigations.

The impact of small groups on pre- and postcopulatory sexual selection in polyandrous populations.

Sexual selection is a key evolutionary force but varies widely between populations. Two key factors that influence sexual selection are the extent to which females copulate with multiple males (polyandry) and variation in the social environment. Increasing research demonstrates populations are structured by complex socio-sexual networks, and the structure of these networks can influence sexual selection by shaping the relationship between male precopulatory mating success and the intensity of postcopulatory competition. However, comparatively less attention has been dedicated to the influence of group structure on sexual selection and how differences in the size of groups may impact on the relative force of pre- and postcopulatory sexual selection in polyandrous populations. The presence of groups (i.e., group structure) and the size of groups varies widely in nature and forms an implicit part of much experimental sexual selection research under laboratory conditions. Here I use simulations of mating competition within populations that vary in the size of groups they contain, to show that variation in group size, and in particular small groups, can influence sexual selection. Specifically, I show that null expectations for the operation of pre- and postcopulatory sexual selection is governed by the size of groups within populations because smaller group sizes constrain the structure of sexual networks leading to reinforcing episodes of pre- and postcopulatory sexual selection. Given broad variation in group structure in nature and the tendency for experimental sexual selection research to study replicate small groups, these effects have implications for our understanding of the operation of sexual selection in polyandrous populations.

A Review and Case Study of 3D Imaging Modalities for Female Amniote Reproductive Anatomy.

Recent advances in non-invasive imaging methods have revitalised the field of comparative anatomy, and reproductive anatomy has been no exception. The reproductive systems of female amniotes present specific challenges, namely their often internal "hidden" anatomy. Quantifying female reproductive systems is crucial to recognising reproductive pathologies, monitoring menstrual cycles, and understanding copulatory mechanics. Here we conduct a review of the application of non-invasive imaging techniques to female amniote reproductive anatomy. We introduce the commonly used imaging modalities of computed tomography (CT) and magnetic resonance imaging (MRI), highlighting their advantages and limitations when applied to female reproductive tissues, and make suggestions for future advances. We also include a case study of micro CT and MRI, along with their associated staining protocols, applied to cadavers of female adult stoats (Mustela erminea). In doing so, we will progress the discussion surrounding the imaging of female reproductive anatomy, whilst also impacting the fields of sexual selection research and comparative anatomy more broadly.

The 150th anniversary ofThe Descent of Man: Darwin and the impact of sex-role reversal on sexual selection research

AbstractThe year 2021 marks the 150th anniversary of the publication of Charles Darwin’s extraordinary book The Descent of Man and Selection in Relation to Sex. Here, we review the history and impact of a single profound insight from The Descent of Man: that, in some few species, females rather than males compete for access to mates. In other words, these species are ‘sex-role reversed’ with respect to mating competition and sexual selection compared to the majority of species in which sexual selection acts most strongly on males. Over the subsequent 150 years, sex-role-reversed species have motivated multiple key conceptual breakthroughs in sexual selection. The surprising mating dynamics of such species challenged scientists’ preconceptions, forcing them to examine implicit assumptions and stereotypes. This wider worldview has led to a richer and more nuanced understanding of animal mating systems and, in particular, to a proper appreciation for the fundamental role that females play in shaping these systems. Sex-role-reversed species have considerable untapped potential and will continue to contribute to sexual selection research in the decades to come.

Sexual selection maintains a female-specific character in a species with dynamic sex roles

Abstract The effects of sexual selection are more conspicuous among male animals, and, as a result, the majority of sexual selection research focuses on males. However, burgeoning evidence suggests that sexual selection also acts on females, and there have been calls for an increased focus on females. Here, we used a multivariate approach to analyze sexual selection in Kawanaphila nartee, a spermatophore gift-giving bushcricket with dynamic sex roles. Early in the breeding season, females compete for males, and, later, when environmental food resources are more abundant, sex roles revert to Darwinian convention. Ear size, which is much greater in females than in males, has been suggested to affect female fitness as females with larger ears are more likely to reach calling males first under sex-role-reversed conditions. We tested this suggestion and found evidence of positive linear and nonlinear correlational selection acting on female ear size early in the breeding season (under reversed sex roles) but not later in the breeding season (under Darwinian sex roles). Interestingly, there was no correlation between mating success and reproductive success (Bateman gradient) at any time during the season. Together, our results indicate that even brief and circumscribed periods of intrasexual competition among females can lead to sexual selection on morphological characters and that this selection may not depend on multiple mating. Considering the wealth of reports in the literature of brief episodes of intrasexual competition among female animals, we recommend increased study of sexual selection acting on females.

Mate Choice and Null Models

Biologists have proposed a variety of explanations for extravagant sexual displays, and controversies over explanations define the history of sexual selection research. Recently, Richard Prum has defended Darwin’s idea that the evolution of sexual displays is driven by arbitrary and nonadaptive preferences of potential mates. Prum argues that this explanation should be the null model for sexual selection research. I show that if we adopted Prum’s proposal, the inferences we could be justified in making are more modest than he claims. I also discuss problems with estimating model parameters that at present prevent his proposal from being useful in practice.

Limits to male reproductive potential across mating bouts in Drosophila melanogaster

Understanding the sources of variation in reproductive fitness is a central goal of sexual selection research. Research investigating factors limiting male reproductive potential typically focus on limited mate availability or mate access. This focus often minimizes the potential relevance of physiological or other limitations on male reproductive potential, in contrast to the emphasis on studying such limitations in females. This gap in knowledge leaves open questions about how variation in male reproductive success emerges across successive mating bouts. Here, we contribute to bridging this gap by examining male reproductive potential across successive matings and across time. To reveal limits to male reproductive potential, and sources of variation in these limits, we measured mating rate and offspring production in Drosophila melanogaster males under conditions in which mate limitation was abrogated and food was abundant. Even under these ideal conditions, we discovered distinct limits to male reproductive potential after just a few mating bouts. After males mated two to five times on a given day, additional matings often resulted in zero progeny. Furthermore, we found nonlinear relationships between the number of females a male mated with and the number of progeny he sired; and these relationships depended on the male's genotype, early life social environment and recent mating experience. These findings suggest that males who obtain more mates do not always sire the most offspring and that males who are highly successful in obtaining mates during one time period may not be able to continue this success on subsequent mating bouts and days. Together, these findings suggest trade-offs between current and future reproduction for males. More broadly, these results highlight how sexual selection studies may be expanded across individuals' lifetimes to develop a fuller picture of how sexual selection shapes variation.

Sexual selection in complex communities: Integrating interspecific reproductive interference in structured populations.

The social structure of populations plays a key role in shaping variation in sexual selection. In nature, sexual selection occurs in communities of interacting species; however, heterospecifics are rarely included in characterizations of social structure. Heterospecifics can influence the reproductive outcomes of intrasexual competition by interfering with intraspecific sexual interactions (interspecific reproductive interference [IRI]). We outline the need for studies of sexual selection to incorporate heterospecifics as part of the social environment. We use simulations to show that classic predictions for the effect of social structure on sexual selection are altered by an interaction between social structure and IRI. This interaction has wide-ranging implications for patterns of sexual conflict and kin-selected reproductive strategies in socially structured populations. Our work bridges the gap between sexual selection research on social structure and IRI, and highlights future directions to study sexual selection in interacting communities.

Increased copulation duration does not necessarily reflect a proportional increase in the number of transferred spermatozoa

Abstract Post-copulatory sexual selection research tends to focus on the numerous adaptations that have evolved to increase the chances of donated spermatozoa fertilizing oocytes. Even though fertilization obviously directly depends on the presence of sufficient, viable spermatozoa, the quantification of the sperm transfer process itself has not received the attention it deserves. Here, we present experimental work on a simultaneously hermaphroditic snail in combination with a review of the literature focussing on the relationship between the duration of copulation and the number of sperm that are transferred. Based on classical work, this relationship is often assumed to be linear, but as we show here this need not be the case. Both our experimental data and the reviewed literature indicate that there are clear instances where the process of sperm transfer is not a linear process, i.e., longer copulation duration does not necessarily imply more transfer of sperm. As we point out, there seems to be a bias in the literature towards investigating this in insects, but other animal groups in which this has been investigated do show similar relationships. To conclude, we discuss how the specific patterns of sperm transfer that have been reported can be biologically interpreted and we caution that simply using copulation duration as a proxy for the number of sperm transferred can be misleading.

Choice of high-quality mates versus avoidance of low-quality mates.

Research in sexual selection assumes that individuals attempt to choose high-quality mates, and that sexual signals evolve to indicate high quality. But it may often be more important to instead discriminate and avoid low-quality mates, thus reducing the likelihood of large penalties in fitness. We show, using simulations, that avoidance of low-quality mates (i.e., rejecting low-quality and accepting either high- or medium-quality mates) evolves in socio-ecological circumstances such as monogamy with moderate opportunities for choice, costly choice, or abundant low-quality mates. We also show that this strategy is qualitatively different from choosing high-quality mates (i.e., preferring high-quality over medium- and low-quality mates). Rather than selecting signals that distinguish high- from low- and medium-quality mates, avoiding low-quality mates selects for signals or cues attuned at discriminating low-quality mates from the remaining (e.g., low-cost signals, absence of signaling mistakes). This may help explain the high diversity of sexual signals in nature, and their high evolutionary turnover with frequent losses and replacements (rather than reductions/increases of the same signal) over evolutionary time.

Operational sex ratio predicts the opportunity and direction of sexual selection across animals.

The operational sex ratio (OSR) has long been assumed to be a key ecological factor determining the opportunity and direction of sexual selection. However, recent theoretical work has challenged this view, arguing that a biased OSR does not necessarily result in greater monopolisation of mates and therefore stronger sexual selection in the mate-limited sex. Hence, the role of the OSR for shaping animal mating systems remains a conundrum in sexual selection research. Here we took a meta-analytic approach to test whether OSR explains interspecific variation in sexual selection metrics across a broad range of animal taxa. Our results demonstrate that the OSR predicts the opportunity for sexual selection in males and the direction of sexual selection in terms of sex differences in both the opportunity for sexual selection and the Bateman gradient (i.e. the selection differential of mating success), as predicted by classic theory.

The evolution of costly mate choice against segregation distorters.

The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well-known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low-quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non-Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control.

Humans as a model species for sexual selection research.

Ever since Darwin, questions about humans have driven sexual selection research. While studies of other organisms are often justified as useful for improving understanding of humans, humans themselves can be useful models. Although humans present some drawbacks as model organisms (complicated societies, slow reproduction and strong ethical constraints on experimental options), humans nonetheless offer many advantages (being abundant, accessible and having detailed historical records for some populations). As an additional challenge, humans exhibit a rather puzzling combination of traits. Some traits (pair-bonding, biparental care and modest sexual dimorphism in body size) suggest selection for monogamous mating, while other traits (including sexual dimorphism in body composition and appearance) suggest selection for polygyny. Such puzzles have motivated research on other species, resulting in a rich set of comparative data that provides insights into humans and other species. Recent studies of visual trait dimorphism suggest that human appearance reflects adaptation for multi-level societies, rather than high levels of polygyny. In addition to biological traits, human cultural traits have undergone rapid evolution. Changes in subsistence strategies profoundly affect opportunities for sexual selection. The enormous variability of human behaviour and ecology provides abundant opportunities to test key hypotheses, and poses challenging puzzles for future research.

Behaviors associated with mating success in the “purring” wolf spider Gladicosa gulosa

AbstractStudies of sexual selection in animal systems frequently use courtship and receptivity behaviors as metrics for mating success, and this is generally built upon data associating such behaviors with mating. Spider systems are becoming increasingly popular in sexual selection research, and the wolf spider Gladicosa gulosa has the potential to help answer unique questions in animal communication. However, this species is understudied, and no quantitative data exist that demonstrate which male and female behaviors may be indicators of mating success. We paired male and female G. gulosa and recorded the behaviors involved in their courtship and mating. We found a number of significant behaviors from both males and females, and we suggest which behaviors/variables are perhaps most predictive of mating success. Beyond building a data‐based foundation for future work, we also suggest that the relationship of certain male and female variables may shed light on some of the more unique features of this species.

Multimodal signalling in estrildid finches: song, dance and colour are associated with different ecological and life-history traits.

Sexual traits (e.g. visual ornaments, acoustic signals, courtship behaviour) are often displayed together as multimodal signals. Some hypotheses predict joint evolution of different sexual signals (e.g. to increase the efficiency of communication) or that different signals trade off with each other (e.g. due to limited resources). Alternatively, multiple signals may evolve independently for different functions, or to communicate different information (multiple message hypothesis). We evaluated these hypotheses with a comparative study in the family Estrildidae, one of the largest songbird radiations, and one that includes many model species for research in sexual selection and communication. We found little evidence for either joint evolution or trade-offs between song and colour ornamentation. Some negative correlations between dance repertoire and song traits may suggest a functional compromise, but generally courtship dance also evolved independently from other signals. Instead of correlated evolution, we found that song, dance and colour are each related to different socio-ecological traits. Song complexity evolved together with ecological generalism, song performance with investment in reproduction, dance with commonness and habitat type, whereas colour ornamentation was shown previously to correlate mostly with gregariousness. We conclude that multimodal signals evolve in response to various socio-ecological traits, suggesting the accumulation of distinct signalling functions.

Sexual Selection: A Short Review on Its Causes and Outcomes, and Activities to Teach Evolution and the Nature of Science

Sexual selection plays an important role in species evolution and speciation, and is fundamental to understanding of biological evolution. In the last decades, research on sexual selection helped understand its causes and impacts in species evolution, sexual dimorphism, and speciation. It also provided interesting examples that can be used to engage students in learning about evolution. Here we review the latest sexual selection research and propose two activities that model evolution by sexual selection. The engaging nature of these activities makes them useful to promote active learning about evolution, the nature of science, and methods used to construct scientific knowledge. Importantly, we address several performance expectations suggested by the Next Generation Science Standards.

The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype-linked fertility hypothesis.

The origin and maintenance of mating preferences continues to be an important and controversial topic in sexual selection research. Leks and lek-like mating systems, where individuals gather in particular spots for the sole purpose of mate choice, are particularly puzzling, because the strong directional selection imposed by mate choice should erode genetic variation among competing individuals and negate any benefit for the choosing sex. Here, we take advantage of the lek-like mating system of the worm pipefish (Nerophis lumbriciformis) to test the phenotype-linked fertility hypothesis for the maintenance of mating preferences. We use microsatellite markers to perform a parentage analysis, along with a mark-recapture study, to confirm that the worm pipefish has an unusual mating system that strongly resembles a female lek, where females display and males visit the lek to choose mates. Our results show that the most highly ornamented females occupy positions near the centre of the breeding area, and males mating with these females receive fuller broods with larger eggs compared to males mating with less-ornamented females. We also conduct a laboratory experiment to show that female ornaments are condition-dependent and honestly signal reproductive potential. Overall, these results are consistent with the predictions of a sex-independent version of the phenotype-linked fertilityhypothesis, as male preference for female ornaments correlates with fertility benefits.

Synergistic selection between ecological niche and mate preference primes diversification.

The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.