Edward H. Morrow

The definition of biological sex has become a renewed focus of societal debate, fuelled by the conflation of biological principles with discussions of human gender diversity. Here, we argue that conceptual clarity critically depends on separating these domains. Drawing on evolutionary theory and empirical evidence, we maintain that biological sex is best defined as a binary classification of male and female reproductive strategies rooted in anisogamy, characterised by the production of two discrete gamete types of different sizes. We stress that gamete size constitutes the ultimate criterion for biological sex and that this definition applies consistently across sexual systems, from separate‐sexed species to hermaphrodites, irrespective of variation in karyotype, hormonal profile, somatic phenotype, or behaviour. Further, we emphasise that evolutionary insights offer a coherent explanation for recurring, though not universal, associations between biological sex and patterns of sex‐specific selection, sexual dimorphism and parental care. We conclude that the definition of biological sex as a binary classification based on gamete size is a powerful scientific framework compatible with the diversity of sexual phenotypes found in anisogamous organisms and distinct from the concept of human gender.

Sexual selection is a major evolutionary force, yet its demographic consequences remain unclear. While experimental studies often report positive effects of sexual selection on traits linked to population performance, comparative studies often find null or negative associations with population persistence. One explanation for this discrepancy is that the demographic consequences of sexual selection depend on ecological context, particularly variation in mortality and fecundity. Here, we used six decades of abundance data and test whether sexual selection predicts population trends across 738 bird species from Europe and North America. We quantify sexual selection using complementary proxies capturing different components of sexual selection: mating system, sexual dichromatism, sexual size dimorphism and relative testes mass. We further assess whether the effect of sexual selection in population trends is mediated by mortality and fecundity. Across all proxies, we found no evidence that sexual selection is associated with population trends. This result is consistent across continents and robust to variation in mortality and fecundity. Our findings suggest that, despite its central role in shaping phenotypic evolution, sexual selection does not translate into consistent effects on long-term population trends at macroecological scales. More broadly, these results highlight a potential disconnect between evolutionary processes and population dynamics.

Trade-offs form a key constraint in many aspects of organismal evolution, though they may help maintain genetic diversity. Late-onset Alzheimer’s disease (LOAD) shows features in common with the male-female health survival paradox: females suffer from higher prevalence and risk, as well as faster rates of cognitive decline while males suffer higher mortality. Though antagonistic pleiotropy could explain the tendency of LOAD to appear late in life, the sexually dimorphic profile suggests a role for intralocus sexual conflict. Using published data on sex-specific genetic associations with LOAD risk, we found evidence for a number of sexually antagonistic loci, where alleles with net negative effects that reduce male risk but increase female risk are more common than alleles with reversed effects. Multiple lines of evidence also suggest there is an inverse relationship between cancer and LOAD risk. The combined effect of sexual antagonism and antagonistic pleiotropy could explain the persistence of alleles that increase LOAD risk in post-reproductive females, if they also reduce cancer risk in males. This framework could be applied to other female-biased late-life conditions, and our results may be useful in informing polygenic risk scores or therapies where genotype-by-sex effects may result in undesired outcomes for one particular sex.

Recombination plays a key role in increasing the efficacy of selection. We investigate whether recombination can also play a role in resolving adaptive conflicts at loci coding for traits shared between the sexes. Errors during recombination events resulting in gene duplications may provide a long-term evolutionary advantage if those loci also experience sexually antagonistic (SA) selection since, after duplication, sex-specific expression profiles will be free to evolve, thereby reducing the load on population fitness and resolving the conflict. The potential advantage of gene duplication may be tempered by the short-term deleterious effects on gamete and zygote survival, which may be tolerable in a species with high reproductive output but not with low reproductive output. We used datasets of candidate SA loci from Drosophila melanogaster and humans to test these ideas. As in humans, sexually antagonistic alleles in flies with net positive effects across the two sexes occurred at higher frequencies than alleles with net negative effects. In flies, higher recombination rates were associated with more intense levels of sexual conflict and genes with paralogues occur in regions with higher recombination rates, indicating gene duplication events are associated with a history of SA selection. Genes experiencing higher levels of conflict also showed both a higher proportion with paralogues and higher numbers of paralogues. Together, our findings reveal multiple lines of evidence for a possible route towards the resolution of an adaptive conflict via gene duplication that is facilitated by higher recombination rates.

Rapid genitalia evolution is believed to be mainly driven by sexual selection. Recently, noncopulatory genital functions have been suggested to exert stronger selection pressure on female genitalia than copulatory functions. In bedbugs (Cimicidae), the impact of the copulatory function can be isolated from the noncopulatory impact. Unlike in other taxa, female copulatory organs have no function in egg-laying or waste-product expulsion. Males perform traumatic mating by piercing the female integument, thereby imposing antagonistic selection on females and suspending selection to morphologically match female genitalia. We found the location of the copulatory organ evolved rapidly, changing twice between dorsal and ventral sides, and several times along the anteroposterior and the left–right axes. Male genital length and shape varied much less, did not appear to follow the positional changes seen in females, and showed no evidence for coevolution. Female genitalia position evolved 1.5 times faster than male genital length and shape and showed little neutral or geographic signals. Instead, we propose that nonmorphological male traits, such as mating behavior, may drive female genitalia morphology in this taxon. Models of genitalia evolution may benefit from considering morphological genital responses to nonmorphological stimuli, such as male mating behavior or copulatory position.

Bateman’s principles, originally a test of Darwin’s theoretical ideas, have since become fundamental to sexual selection theory and vital to contextualizing the role of anisogamy in sex differences of precopulatory sexual selection. Despite this, Bateman’s principles have received substantial criticism, and researchers have highlighted both statistical and methodological errors, suggesting that Bateman’s original experiment contains too much sampling bias for there to be any evidence of sexual selection. This study uses Bateman’s original method as a template, accounting for two fundamental flaws in his original experiments, (a) viability effects and (b) a lack of mating behavior observation. Experimental populations of Drosophila melanogaster consisted of wild-type focal individuals and nonfocal individuals established by backcrossing the brown eye (bw-) eye-color marker—thereby avoiding viability effects. Mating assays included direct observation of mating behavior and total number of offspring, to obtain measures of mating success, reproductive success, and standardized variance measures based on Bateman’s principles. The results provide observational support for Bateman’s principles, particularly that (a) males had significantly more variation in number of mates compared with females and (b) males had significantly more individual variation in total number of offspring. We also find a significantly steeper Bateman gradient for males compared to females, suggesting that sexual selection is operating more intensely in males. However, female remating was limited, providing the opportunity for future study to further explore female reproductive success in correlation with higher levels of remating.

Sexual antagonism is thought to be an important selective force in multiple evolutionary processes, but very few examples of the genes involved are known. Such a deficit of loci could partially be explained by the lack of overlap in terminology between scientific disciplines. Following a similar review in humans, we searched systematically for studies that described genes with sexually antagonistic or sex‐opposite effects in any taxa, using terms designed to capture alternative descriptions of sexual antagonism. Despite drawing on a potentially very large pool of studies we found only eight articles, which between them described seven candidate variants, five of these were gene knockouts. In every case, the variants had net negative effects on the focal trait. One locus was independently validated between studies, but in comparison to previous data on variants in humans and the fruit‐fly, the studies generally suffered from small sample sizes, with concomitant high variance. Our review highlights the radically different effects that gene deletions can have on males and females, where the beneficial effects seen in one sex may facilitate the evolution of gene loss. We searched systematically for genetic variants with sexually antagonistic or sex‐opposite effects in any taxa. Of 2116 articles, we found seven candidate variants, five of which were gene knockouts. Our review highlights the radically different effects that gene deletions can have on males and females, where the beneficial effects seen in one sex may facilitate the evolution of gene loss.

Sexual selection is considered the major driver for the evolution of sex differences. However, the eco-evolutionary dynamics of sexual selection and their role for a population’s adaptive potential to respond to environmental change have only recently been explored. Theory predicts that sexual selection promotes adaptation at a low demographic cost only if sexual selection is aligned with natural selection and if net selection is stronger on males compared to females. We used a comparative approach to show that net selection is indeed stronger in males and provide preliminary support that this sex bias is associated with sexual selection. Given that both sexes share the vast majority of their genes, our findings corroborate the notion that the genome is often confronted with a more stressful environment when expressed in males. Collectively, our study supports one of the long-standing key assumptions required for sexual selection to bolster adaptation, and sexual selection may therefore enable some species to track environmental change more efficiently.

An evolutionary model for sex differences in disease risk posits that alleles conferring higher risk in one sex may be protective in the other. These sexually antagonistic (SA) alleles are predicted to be maintained at frequencies higher than expected under purifying selection against unconditionally deleterious alleles, but there are apparently no examples in humans. Discipline-specific terminology, rather than a genuine lack of such alleles, could explain this disparity. We undertook a two-stage review of evidence for SA polymorphisms in humans using search terms from (i) evolutionary biology and (ii) biomedicine. While the first stage returned no eligible studies, the second revealed 51 genes with sex-opposite effects, 22 increased disease risk or severity in one sex but protected the other. Those with net positive effects occurred at higher frequencies. None were referred to as SA. Our review reveals significant communication barriers to fields as a result of discipline-specific terminology. This article is protected by copyright. All rights reserved

Sexual selection is considered the major driver for the evolution of manifold sex differences. However, the eco-evolutionary dynamics of sexual selection and their role for a population’s adaptive potential to respond to environmental change have only recently been explored. Theory predicts that sexual selection promotes adaptation at a low demographic cost only if net selection is stronger on males compared to females. We used a comparative approach to show that net selection is indeed stronger in males in species prone to intense sexual selection. Given that both sexes share the vast majority of their genes, our findings corroborate the notion that the genome is often confronted with a more stressful environment when expressed in males. Collectively, our study supports a long-standing key assumption required for sexual selection to bolster adaptation, and intense sexual selection may therefore enable some species to track environmental change more efficiently. One sentence summary Comparative study finds support for stronger net selection in males.