'With all these exalted powers – Man still bears in his bodily frame the indelible stamp of his lowly origin'

In The Origin of Species, 1859, Charles Darwin refused to discuss human evolution, believing the subject too ‘surrounded with prejudices’. He had been reworking his notes since the 1830s, but only with much trepidation did he finally publish The Descent of Man in 1871. The book notoriously put apes in our family tree and made the races one family, diversified by ‘sexual selection’ - Darwin’s provocative theory that female choice among competing males leads to diverging racial characteristics. Named by Sigmund Freud as ‘one of the ten most significant books’ ever written, Darwin’s Descent of Man continues to shape the way we think about what it is that makes us uniquely human.

In their introduction, James Moore and Adrian Desmond, acclaimed biographers of Charles Darwin, call for a radical re-assessment of the book, arguing that its core ideas on race were fired by Darwin’s hatred of slavery. This reprint of the second and definitive edition also contains suggestions for further reading, a chronology, and biographical sketches of prominent individuals.

The Descent of Man, and Selection in Relation to Sex by Charles Darwin

BACKGROUND We are witnessing renewed debates regarding definitions and boundaries of human gender/sex, where lines of genetics, gonadal hormones, and secondary sex characteristics are drawn to defend strict binary categorizations, with attendant implications for the acceptability and limits of gender identity and diversity. AIMS Many argue for the need to recognize the entanglement of gender/sex in humans and the myriad ways that gender experience becomes biology; translating this theory into practice in human biology research is essential. Biological anthropology is well poised to contribute to these societal conversations and debates. To do this effectively, a reconsideration of our own conceptions of gender/sex, gender identity, and sexuality is necessary. METHODS In this article, we discuss biological variation associated with gender/sex and propose ways forward to ensure we are engaging with gender/sex diversity. We base our analysis in the concept of "biological normalcy," which allows consideration of the relationships between statistical distributions and normative views. We address the problematic reliance on binary categories, the utilization of group means to represent typical biologies, and document ways in which binary norms reinforce stigma and inequality regarding gender/sex, gender identity, and sexuality. DISCUSSION AND CONCLUSIONS We conclude with guidelines and methodological suggestions for how to engage gender/sex and gender identity in research. Our goal is to contribute a framework that all human biologists can use, not just those who work with gender or sexually diverse populations. We hope that in bringing this perspective to bear in human biology, that novel ideas and applications will emerge from within our own discipline.

Challenging the binary: Gender/sex and the bio-logics of normalcy.

What is a pair bond

Interactions between species can alter selection on sexual displays used in mate choice within species. Here we study the epicuticular pheromones of two Drosophila species that overlap partially in geographic range and are incompletely reproductively isolated. Drosophila subquinaria shows a pattern of reproductive character displacement against Drosophila recens, and partial behavioral isolation between conspecific sympatric versus allopatric populations, whereas D. recens shows no such variation in mate choice. First, using manipulative perfuming experiments, we show that females use pheromones as signals for mate discrimination both between species and among populations of D. subquinaria. Second, we show that patterns of variation in epicuticular compounds, both across populations and between species, are consistent with those previously shown for mating probabilities: pheromone compositions differ between populations of D. subquinaria that are allopatric versus sympatric with D. recens, but are similar across populations of D. recens regardless of overlap with D. subquinaria. We also identify differences in pheromone composition among allopatric regions of D. subquinaria. In sum, our results suggest that epicuticular compounds are key signals used by females during mate recognition, and that these traits have diverged among D. subquinaria populations in response to reinforcing selection generated by the presence of D. recens.

https://www.onlinelibrary.wiley.com/doi/pdf/10.1111/evo.12335

Reproductive character displacement of epicuticular compounds and their contribution to mate choice in drosophila subquinaria and drosophila recens

Over the past century, ecologists have attempted to understand patterns of species diversity by showing stable coexistence arising from a baseline expectation of competitive exclusion. This expectation stems from an explicit assumption of resource scarcity and implicit assumptions of Malthusian struggle and winner-takes-all dynamics. Fidelity to the competitive exclusion principle (CEP) presents species diversity as a paradox: if species compete for limited resources, how can they coexist? In this article, we investigate the contradiction between the theoretical expectation of competitive exclusion and the empirical prevalence of multispecies communities. We trace the persistence of the CEP in ecological research despite numerous challenges and explore publishing trends suggesting that this framework has resulted in a disproportionate focus on competition and exclusion in contemporary research. From a critical science studies perspective, we analyze the sociopolitical factors that have contributed to these patterns. We argue that we must excavate the ideological foundation on which competition-based coexistence research has been built to move beyond the current perceived “diversity paradox.” To that end, we propose shifting the baseline expectation of coexistence research, introducing the notion of a coexistence principle, which positions the persistence of multispecies communities as the rule rather than the exception in nature.

Moving beyond the “Diversity Paradox”: The Limitations of Competition-Based Frameworks in Understanding Species Diversity

Same-sex sexual behaviour (SSB) has been recorded in over 1,500 animal species with a widespread distribution across most major clades. Evolutionary biologists have long sought to uncover the adaptive origins of 'homosexual behaviour' in an attempt to resolve this apparent Darwinian paradox: how has SSB repeatedly evolved and persisted despite its presumed fitness costs? This question implicitly assumes that 'heterosexual' or exclusive different-sex sexual behaviour (DSB) is the baseline condition for animals, from which SSB has evolved. We question the idea that SSB necessarily presents an evolutionary conundrum, and suggest that the literature includes unchecked assumptions regarding the costs, benefits and origins of SSB. Instead, we offer an alternative null hypothesis for the evolutionary origin of SSB that, through a subtle shift in perspective, moves away from the expectation that the origin and maintenance of SSB is a problem in need of a solution. We argue that the frequently implicit assumption of DSB as ancestral has not been rigorously examined, and instead hypothesize an ancestral condition of indiscriminate sexual behaviours directed towards all sexes. By shifting the lens through which we study animal sexual behaviour, we can more fruitfully examine the evolutionary history of diverse sexual strategies.

An alternative hypothesis for the evolution of same-sex sexual behaviour in animals

Most animal species use distinctive courship patterns to choose among potential mates. Over time, the sensory signaling and preferences used during courtship can diverge among groups that are reproductively isolated. This divergence of signal traits and preferences is thought to be an important cause of behavioral isolation during the speciation process. Here, we examine the sensory modalities used in courtship by two closely related species, Drosophila subquinaria and Drosophila recens, which overlap in geographic range and are incompletely reproductively isolated. We use observational studies of courtship patterns and manipulation of male and female sensory modalities to determine the relative roles of visual, olfactory, gustatory, and auditory signals during conspecific mate choice. We find that sex-specific, species-specific, and population-specific cues are used during mate acquisition within populations of D. subquinaria and D. recens. We identify shifts in both male and female sensory modalities between species, and also between populations of D. subquinaria. Our results indicate that divergence in mating signals and preferences have occurred on a relatively short timescale within and between these species. Finally, we suggest that because olfactory cues are essential for D. subquinaria females to mate within species, they may also underlie variation in behavioral discrimination across populations and species.

https://www.onlinelibrary.wiley.com/doi/pdf/10.1002/ece3.477

Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens

Leptin regulates song effort in Neotropical singing mice (Scotinomys teguina)

1Miller Institute for Basic Research in Science, University of California Berkeley, Berkeley, CA, USA. 2Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, USA. 3Center for Reproductive Evolution, Department of Biology, Syracuse University, Syracuse, NY, USA. 4School of Forestry & Environmental Studies, Yale University, New Haven, CT, USA. 5Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA. ✉e-mail: julia.monk@yale.edu In Monk et al.1, we hypothesized that indiscriminate sexual behaviour is the ancestral condition for sexually reproducing animals and that this, coupled with the potentially low costs of same-sex sexual behaviour (SSB), can contribute to explaining the prevalence of SSB across extant animals. First, it is important to reiterate that we defined different-sex sexual behaviour (DSB) and SSB as discrete behavioural interactions, which are not synonymous with an individual’s ‘orientation’ or ‘attraction’ (as used by Dickins and Rahman2 and Clive et al.3 in their correspondences). Given the strong connotations of these last two phrases in human contexts, their imprecise application to animals can result in the unconscious projection of human values onto animals, to the detriment of both accurate science and just society4. Second, we described an ancestral state of indiscriminate sexual behaviour that is a combination of DSB and SSB (Fig. 2 in Monk et al.1), and not a distinct category of sexual behaviour that preceded DSB and SSB (as interpreted by Clive et al.3 and Dickins and Rahman2). Thus, our hypothesis of ancestral indiscriminate sexual behaviour predicts a more parsimonious scenario than the repeated de novo evolution of SSB from a background of exclusive DSB. Third, our hypothesis does not preclude or obviate the relevance of any particular adaptive or non-adaptive explanation for SSB to any particular taxon. As we stated in Monk et al.1, “Herein lies the crux of our argument: any individual adaptive or non-adaptive hypothesis put forward to explain the ‘purpose’ of SSB in animals may well explain its persistence, including the secondary nonreproductive functions for which SSB has been co-opted. However, the origins of SSB may lie not in recent evolutionary events producing those functions but in the earliest forms of sexual behaviours.”. Many arguments made in both correspondences are addressed directly by this statement. Clive et al.3 state that “no published research, as far as we know, has asserted an ancestral state of exclusive DSB.”. This is consistent with our stance in Monk et al.1, where we argued that the assumption of ancestral DSB has been implicit, with few researchers paying explicit attention to the evolutionary origins of sexual behaviour more broadly than in their taxon of interest (but see refs. 5–7). Nevertheless, an implicit assumption is still a stance, and to discuss the evolution of a trait from a state where the trait is presumed absent is inherently, if implicitly, to assume that the trait is derived. Considering the ancestral states of sexual behaviours is critical to interpreting the evolution of SSB because whether a trait is rare or common in an ancestral population can be profoundly consequential for its subsequent evolution. While we previously focused on a single origin of sexual behaviour, it is likely that sexual behaviours evolved multiple times. Our hypothesis would be applicable to each independent origin of sexual behaviours (Box 2 in Monk et al.1). Moreover, although it was extremely valuable to reference Parker’s model8 for the evolution of sexual behaviours to help conceptualize the characteristics of the ancestral state, that model investigates a specific question of the evolution of mobility and female targeting (that is, exclusive DSB) from an ancestral strategy of broadcast spawning. Our hypothesis is thus distinct from Parker’s model in considering the evolution of specificity of sexual behaviours more broadly. The notion of SSB as a ‘paradox’, which motivates most existing hypotheses for SSB9, reveals the implicit assumption that SSB is highly costly—SSB is paradoxical only if it is assumed to be highly costly. It is this baseline assumption that we make explicit, and contest. Previous research7,10–14, cited in Monk et al.1, has shown empirically that SSB may not be costly, although many of these papers nevertheless describe SSB as paradoxical. We note that the study of Gavrilets and Rice15 was designed to model the minimum benefit and maximum cost necessary for an allele increasing the frequency of SSB to invade a purely DSB population, thus making similar assumptions to those that we challenge. Notably, in Monk et al.1, we use ‘indirect’ benefits not in the Hamiltonian sense of benefiting relatives as opposed to oneself, but rather to refer to any beneficial outcome of a sexual behaviour other than fertilization and the production of offspring. Clive et al.3 suggest that our usage is confusing, and we appreciate this opportunity for clarification. Our hypothesis of ancestral indiscriminate sexual behaviour is not equivalent to the existing non-adaptive ‘mistaken identity’ hypothesis. The mistaken identity hypothesis suggests that SSB is a consequence of errors in identifying the sex of a potential mating partner (that is, an imperfect execution of mate selection) and would always be selected against, although the response to selection would be constrained by signalling and perceptual limitations. In contrast, our hypothesized evolutionary scenario proposes that SSB would be selected against only in taxa where the costs of SSB became high, and in many environmental situations, these costs may not be very high. Clive et al.3 imply that selection will always be able to remove constraint if the costs of SSB are high, and thus claim that hypotheses for SSB invoking constraint are assuming the costs of SSB to be low. However, selection cannot always eliminate constraint, regardless of how beneficial it might be to do so16. Past research has investigated adaptive functions and proximate causes of SSB, but has largely not considered SSB within a larger phylogenetic context. This lack of explicit engagement with evolutionary origins has allowed the discussion of SSB to continue A. Kamath et al. reply

A. Kamath et al. reply.

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An alternative hypothesis for the evolution of same-sex sexual behaviour in animals

Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens

Leptin regulates song effort in Neotropical singing mice (Scotinomys teguina)

A. Kamath et al. reply.