Borrowed plumes: mimetic powers and the polymorphism of humans

In this paper, I speculate on imitation??s role in language development and, more significantly, on its connection to sexual selection. My analysis is grounded in an interpretation of Darwin??s Descent of Man. In addition to observing imitation??s role in language development according to the argument of the Descent, I explore the ability of human beings that allows for the imitation of both the beautiful and the terrible or repulsive. I suggest that humans, in their appreciation of the beautiful and formidable characters produced by a process of sexual selection, can appropriate these things in order to adorn themselves, thus imitating other non-human animals. This capacity points to a form of polymorphism manifest in human beings that is grounded in a psychological fluidity. Human beings, like birds, also have the power to use song in order to charm and challenge. Song and music provide the means by which imitation as seen in language development and sexual selection are intertwined, thus providing the important connection between the two main foci of my paper.     

Darwin's explanation of races by means of sexual selection

In Darwin's Sacred Cause, Adrian Desmond and James Moore contend that "Darwin would put his utmost into sexual selection because the subject intrigued him, no doubt, but also for a deeper reason: the theory vindicated his lifelong commitment to human brotherhood" (2009: p. 360). Without questioning Desmond and Moore's evidence, I will raise some puzzles for their view. I will show that attention to the structure of Darwin's arguments in the Descent of Man shows that they are far from straightforward. As Desmond and Moore note, Darwin seems to have intended sexual selection in non-human animals to serve as evidence for sexual selection in humans. However, Darwin's account of sexual selection in humans was different from the canonical cases that Darwin described at great length. If explaining the origin of human races was the main reason for introducing sexual selection, and if sexual selection was a key piece of Darwin's anti-slavery arguments, then it is puzzling why Darwin would have spent so much time discussing cases that did not really support his argument for the origin of human races, and it is also puzzling that his argument for the origin of human races would be so (atypically) poor.     

Darwin on woman

In his 1871 book The Descent of Man, Darwin exposed the idea of sexual selection as a major principle of human evolution. His main hypothesis, which was already briefly presented in The Origin of Species, is that there exists, besides “natural selection”, another form of selection, milder in its effect, but no less efficient. This selection is operated by females to mate and reproduce with some partners that are gifted with more qualities than others, and more to their taste. At more evolved stages, sexual selection was exerted by men who became able to choose the women most attractive to their taste. However, Darwin insists, sexual selection in the human species is limited by a certain number of cultural practices. If Darwin's demonstration sometimes carried the prejudices of his times regarding gender differences he was the first who took into account the importance of sexual choices in his view on evolution, and who insisted on the evolutionary role of women at the dawn of humanity. Thus, he opened the space for a rich reflection, which after him was widely developed and discussed in anthropological and gender studies.     

Sexual selection: Another Darwinian process

Why was sexual selection so important to Darwin? And why was it de-emphasized by almost all of Darwin's followers until the second half of the 20th century? These two questions shed light on the complexity of the scientific tradition named “Darwinism”. Darwin's interest in sexual selection was almost as old as his discovery of the principle of natural selection. From the beginning, sexual selection was just another “natural means of selection”, although different from standard “natural selection” in its mechanism. But it took Darwin 30 years to fully develop his theory, from the early notebooks to the 1871 book The Descent of Man, and Selection in Relation to Sex. Although there is a remarkable continuity in his basic ideas about sexual selection, he emphasized increasingly the idea that sexual selection could oppose the action of natural selection and be non adaptive. In time, he also gave more weight to mate choice (especially female choice), giving explicit arguments in favor of psychological notions such as “choice” and “aesthetic sense”. But he also argued that there was no strict demarcation line between natural and sexual selection, a major difficulty of the theory from the beginning. Female choice was the main reason why Alfred Russel Wallace, the co-discoverer of the principle of natural selection, engaged in a major controversy with Darwin about sexual selection. Wallace was suspicious about sexual selection in general, trying to minimize it by all sorts of arguments. And he denied entirely the existence of female choice, because he thought that it was both unnecessary and an anthropomorphic notion. This had something to do with his spiritualist convictions, but also with his conception of natural selection as a sufficient principle for the evolutionary explanation of all biological phenomena (except for the origin of mind). This is why Wallace proposed to redefine Darwinism in a way that excluded Darwin's principle of sexual selection. The main result of the Darwin–Wallace controversy was that most Darwinian biologists avoided the subject of sexual selection until at least the 1950 s, Ronald Fisher being a major exception. This controversy still deserves attention from modern evolutionary biologists, because the modern approach inherits from both Darwin and Wallace. The modern approach tends to present sexual selection as a special aspect of the theory of natural selection, although it also recognizes the big difficulties resulting from the inevitable interaction between these two natural processes of selection. And contra Wallace, it considers mate choice as a major process that deserves a proper evolutionary treatment. The paper's conclusion explains why sexual selection can be taken as a test case for a proper assessment of “Darwinism” as a scientific tradition. Darwin's and Wallace's attitudes towards sexual selection reveal two different interpretations of the principle of natural selection: Wallace's had an environmentalist conception of natural selection, whereas Darwin was primarily sensitive to the element of competition involved in the intimate mechanism of any natural process of selection. Sexual selection, which can lack adaptive significance, reveals this exemplarily.     

Sexually selected traits predict patterns of species richness in a diverse clade of suboscine birds

Whether sexual selection acts as an "engine of speciation" is controversial. Some studies suggest that it promotes the evolution of reproductive isolation, while others find no relationship between sexual selection and species richness. However, the explanatory power of previous models may have been constrained because they employed coarse-scale, between-family comparisons and used mating systems and morphological cues as surrogates for sexual selection. In birds, an obvious missing predictor is song, a sexually selected trait that functions in mate choice and reproductive isolation. We investigated the extent to which plumage dichromatism and song structure predicted species richness in a diverse family of Neotropical suboscine birds, the antbirds (Thamnophilidae). These analyses revealed a positive relationship between the intensity of sexual selection and diversity: genera with higher levels of dichromatism and lower-pitched, more complex songs contained greater numbers of species. This relationship held when controlling for phylogeny and was strengthened by the inclusion of subspecies, suggesting that sexual selection has played a role in the diversification of antbirds. This is the first study to reveal correlations between song structure and species diversity, emphasizing the importance of acoustic signals, and within-family analyses, in comparative studies of sexual selection.     

Evolution of sexual dichromatism in relation to nesting habits in European passerines: a test of Wallace's hypothesis

Wallace proposed in 1868 that natural rather than sexual selection could explain the striking differences in avian plumage dichromatism. Thus, he predicted that nesting habits, through their association with nest predation, could drive changes in sexual dichromatism by enabling females in cavity nesters to become as conspicuous as males, whereas Darwin (1871, The Descent of Man and Selection in Relation to Sex, John Murray, London) argued that sexual selection was the sole explanation for dichromatism. Sexual dichromatism is currently used as indicating the strength of sexual selection, and therefore testing Wallace's claim with modern phylogentically controlled methodologies is of prime interest for comparing the roles of natural and sexual selection in affecting the evolution of avian coloration. Here, we have related information on nest attendance, sexual dichromatism and nesting habits (open and cavity nesting) to male and female plumage conspicuousness in European passerines. Nest incubation attendance does not explain male or female plumage conspicuousness but nest type does. Moreover, although females of monochromatic and cavity nesting species are more conspicuous than females of other species, males of monochromatic and open nesting species are those with more cryptic plumage. Finally, analyses of character evolution suggest that changes in nesting habits influence the probability of changes in both dichromatism and plumage conspicuousness of males but do not significantly affect those in females. These results strongly suggest a role of nesting habits in the evolution of plumage conspicuousness of males, and a role for sexual selection also in females, both factors affecting the evolution of sexual dichromatism. We discuss our findings in relation to the debate that Darwin and Wallace maintained more than one century ago on the importance of natural and sexual selection in driving the evolution of plumage conspicuousness and sexual dichromatism in birds, and conclude that our results partly support the evolutionary scenarios envisaged by both extraordinary scientists.     

Darwin and sexual selection: One hundred years of misunderstanding

Darwin's book on the Descent of Man and Selection in Relation to Sex (1871) is often viewed as the continuation of TheOrigin of Species published 12 years earlier (1859), both because of the implicit parallelism between natural selection and sexual selection, and because Darwin himself presents the book as developing a subject (man) which he intentionally omitted in the Origin. But the Descent can also be viewed as the continuation of his book on Variation published three years earlier (1868). Firstly because Darwin's hypothesis of pangenesis links the selection process to the origin of variation through use and disuse, an idea underlying his speculations on the origin of moral sense in humans. Second because like the action of the horticulturist on his domestic crops, sexual selection exerted by one sex on the other sex can develop fancy traits that are not easily accounted for by their utility to the selected organism itself, such as artistic taste, pride, courage, and the morphological differences between human populations. These traits are difficult to reconcile with pangenesis. They add up to other contradictions of the book possibly resulting from Darwin's erroneous inference about the mechanism of inheritance, like those on the determination of sex-ratio, or the confusion between individual adaptation and the advantage to the species. These inconsistencies inaugurate a weakening of the Darwinian message, which will last 50 years after his death. They contributed to the neglect of sexual selection for a century. Darwin however maintained a logical distinction between evolutionary mechanisms and hereditary mechanisms, and an epistemological distinction between evolutionary theory and Pangenesis hypothesis. In the modern context of Mendelian genetics, Darwin's sexual selection retrospectively appears as luminous an idea in its pure principle as natural selection, even though the mechanisms governing the evolution of sexual choice in animals remain largely unresolved.     

The sight of the peacock’s tail makes me sick: The early arguments on sexual selection

Why does a peacock have a beautiful train, while a peahen is sober without such flamboyance? Darwin proposed the theory of sexual selection to explain the differences between the sexes of the same species. Recently the study of sexual selection has been one of the most flourishing areas in evolutionary biology. However, the theory met with great resistance from biologists since the publication of the idea and the history of the theory included a lot of misunderstanding and confusion. There are several reasons for this. First, classical Darwinism failed to recognize social competition as an important selective force. Second, the good-for-the-species argument, which persisted in the days after Darwin, made the sexual selection argument more difficult to understand. Compared to the discussions on animals, Darwin’s argument on human sex differences is not satisfactory. The reason probably lies in the debate over human racial differences which prevailed in the 19th century.     

Sex-specific ecomorphological variation and the evolution of sexual dimorphism in dwarf chameleons (Bradypodion spp.)

Natural selection can influence the evolution of sexual dimorphism through selection for sex-specific ecomorphological adaptations. The role of natural selection in the evolution of sexual dimorphism, however, has received much less attention than that of sexual selection. We examined the relationship between habitat structure and both male and female morphology, and sexual dimorphism in size and shape, across 21 populations of dwarf chameleon (genus Bradypodion). Morphological variation in dwarf chameleons was strongly associated with quantitative, multivariate aspects of habitat structure and, in most cases, relationships were congruent between the sexes. However, we also found consistent relationships between habitat and sexual dimorphism. These resulted from both differences in magnitude of ecomorphological relationships that were otherwise congruent between the sexes, as well as in sex-specific ecomorphological adaptations. Our study provides evidence that natural selection plays an important role in the evolution of sexual dimorphism.     

Separated at Birth: The Interlinked Origins of Darwin’s Unconscious Selection Concept and the Application of Sexual Selection to Race

This essay traces the interlinked origins of two concepts found in Charles Darwin’s writings: “unconscious selection,” and sexual selection as applied to humanity’s anatomical race distinctions. Unconscious selection constituted a significant elaboration of Darwin’s artificial selection analogy. As originally conceived in his theoretical notebooks, that analogy had focused exclusively on what Darwin later would call “methodical selection,” the calculated production of desired changes in domestic breeds. By contrast, unconscious selection produced its results unintentionally and at a much slower pace. Inspiration for this concept likely came from Darwin’s early reading of works on both animal breeding and physical ethnology. Texts in these fields described the slow and unplanned divergence of anatomical types, whether animal or human, under the guidance of contrasting ideals of physical perfection. These readings, it is argued, also led Darwin to his theory of sexual selection as applied to race, a theme he discussed mainly in his book The Descent of Man (1871). There Darwin described how the racial version of sexual selection operated on the same principle as unconscious selection. He thereby effectively reunited these kindred concepts.     

Phylogenetic analyses of primate size evolution: the consequences of sexual selection

We have analysed the relationship between primate mating system, size and size dimorphism by utilizing several phylogenetically based methods. An independent contrast analysis of male and female size (log weight) showed that these are tightly correlated and that size dimorphism is not a simple allometric function of size. We found no relationship between mating system and sexual dimorphism in strepsirhines but a strong relationship in haplorhines. By matched-pairs analysis, where sister groups were matched according to whether the mating system predicted higher or lower intrasexual selection for male size, haplorhine species in more polygynous clades (with a predicted higher sexual selection) were significantly more dimorphic, had larger males, and also, but to a lesser degree, larger females. Both independent contrast and matched-pairs analyses are non-directional and correlational. By using a directional test we investigated how a transition in mating system affects size and dimorphism. Here, each observation is the sum of changes in dimorphism or size in a clade that is defined by a common origin of a mating system. Generally, dimorphism, as well as male and female size, increased after an expected increase in sexual selection, and decreased after an expected decrease in sexual selection. The pattern was, however, not significant for all of the alternative character reconstructions. In clades with an expected increase in sexual selection, male size increased more than female size. This pattern was significant for all character reconstructions. The directional investigation indicates that the magnitude of change in haplorhine dimorphism is larger after an increase in sexual selection than after a decrease, and, for some reconstructions, that the magnitude of size increase is larger than the magnitude of size decrease for both sexes. Possible reasons for these patterns are discussed, as well as their implications as being one possible mechanism behind Cope's rule, i.e. general size increase in many phylogenetic lineages.     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

No evidence that sexual selection is an 'engine of speciation' in birds

Abstract Sexual selection has been implicated as having a role in promoting speciation, as it should increase the rate of evolution of reproductive isolation, and there is some comparative evidence that sexual selection may be related to imbalances in clade size seen in resolved phylogenies. By employing a new comparative method we are able to investigate the role of sexual selection in explaining the patterns of species richness across birds. We used data for testes size as an index of post‐mating sexual selection, and sexual size dimorphism and sexual dichromatism as indices of pre‐mating sexual selection. These measures were obtained for 1031 species representing 467 genera. None of the variables investigated explained the patterns of species richness. As sexual selection may also increase extinction rates, the net effect on species richness in any given clade will depend on the balancing effects of sexual selection upon speciation and extinction rates. We suggest that variance across clades in this balance may have resulted in the lack of a relationship between species richness and sexual selection seen in birds.     

QUANTITATIVE GENETICS OF SEXUAL DIMORPHISM IN HUMAN BODY SIZE

A classical data set is used to predict the effect of selection on sexual dimorphism and on the population means of three characters—stature, span, and cubit—in humans. Given selection of equal intensity, the population means of stature and of cubit should respond more than 60 times as fast as dimorphism in these characters. The population mean of span should also respond far more rapidly than dimorphism, but no numerical estimate of the ratio of these rates was possible. These results imply that sexual dimorphism in these characters can evolve only very slowly. Consequently, hypotheses about the causes of sexual dimorphism cannot be tested by comparing the dimorphism of different human societies. It has been suggested that primate sexual dimorphism may be an allometric response to selection for larger body size. We show that such selection can indeed generate sexual dimorphism, but that this effect is too weak to account for the observed relationship between dimorphism and body size in primates.     

Sexual selection and the risk of extinction in mammals

Sexual selection is commonly envisaged as a force working in opposition to natural selection, because extravagant or exaggerated traits could apparently have never evolved via natural selection alone. There is good evidence that a selection load imposed by sexual selection may be eased experimentally by restricting the opportunity for it to operate. Sexual selection could therefore potentially play an important role in influencing the risk of extinction that a population faces, thereby contributing to the apparent selectivity of extinctions. Conversely, recent theory predicts that the likelihood of extinction may decrease when sexual selection is operating because it could accelerate the rate of adaptation in concert with natural selection. So far, comparative evidence (coming mostly from birds) has generally indicated support for the former scenario, but the question remains open. The aim of this study was therefore to examine whether the level of sexual selection (measured as residual testes mass and sexual size dimorphism) was related to the risk of extinction that mammals are currently experiencing. We found no evidence for a relationship between these factors, although our analyses may have been confounded by the possible dominating effect of contemporary anthropogenic factors.     

Increase in song frequency decreases spermatophore size: correlative evidence of a macroevolutionary trade-off in katydids (Orthoptera: Tettigoniidae)

In many katydids, the male feeds his mate with a large gelatinous spermatophore. Males of most species also produce elaborate calling songs. We predicted a negative relationship between spermatophore size and call frequency because of trade-offs between these two costly traits. Our comparative analysis controlling phylogeny and body size supported this prediction. Although call frequency is expected to decrease with increasing body size, after controlling for phylogeny, both variables were not related. Finally, given that song frequency and spermatophore size are likely targets of sexual selection, we examined the relationship between these variables and sexual size dimorphism (SSD) which can be influenced by sexual selection on body size. We found that only female body size was positively related to SSD, suggesting that natural and/or sexual selection on female body size may be stronger than sexual selection on male and spermatophore size.     

Sexual selection and sperm competition in primates: What are male genitalia good for?

One hundred twenty-five years ago, in The Descent of Man and Selection in Relation to Sex,¹ Charles Darwin proposed the theory of sexual selection, as distinct from natural selection, to explain why, in some species, males have such magnificent ornaments and, in other species, such impressive weapons. He suggested two processes, which we now term female choice and male-male competition: either females choose particularly ornate males or, alternatively, relatively passive females accept the winner of fights among males. By now, knowledge of species in which the females are more brightly colored or aggressive than males has led to a more general formulation of the principle of sexual selection, in which, instead of “females”, we write “the sex with the lower potential reproductive rate”, and, instead of “male”, “the sex with the higher potential reproductive rate”.²     

Sexual selection and the risk of extinction in birds

The relationship between sexual selection and extinction risk has rarely been investigated. This is unfortunate because extinction plays a key role in determining the patterns of species richness seen in extant clades, which form the basis of comparative studies into the role that sexual selection may play in promoting speciation. We investigate the extent to which the perceived risk of extinction relates to four different estimates of sexual selection in 1030 species of birds. We find no evidence that the number of threatened species is distributed unevenly according to a social mating system, and neither of our two measures of pre-mating sexual selection (sexual dimorphism and dichromatism) was related to extinction risk, after controlling for phylogenetic inertia. However, threatened species apparently experience more intense post-mating sexual selection, measured as testis size, than non-threatened species. These results persisted after including body size as a covariate in the analysis, and became even stronger after controlling for clutch size (two known correlates of extinction risk). Sexual selection may therefore be a double-edged process-promoting speciation on one hand but promoting extinction on the other. Furthermore, we suggest that it is post-mating sexual selection, in particular, that is responsible for the negative effect of sexual selection on clade size. Why this might be is unclear, but the mean population fitness of species with high intensities of post-mating sexual selection may be especially low if costs associated with multiple mating are high or if the selection load imposed by post-mating selection is higher relative to that of pre-mating sexual selection.     

The design of complex sexual traits in male barn swallows: associations between signal attributes

Variation in the expression of sexually selected traits among individuals is widely investigated on the premise that these traits evolved to signal male quality. Significant repeatabilities of sexual signals and their associations with condition, mating success, survivorship and age may be the signatures of sexual selection. However, little is known about the relationship between these sexual attributes. Here we studied 28 acoustic and visual traits in the barn swallow, Hirundo rustica, that may potentially function in sexual selection. Based on effect sizes calculated at the between-individual level, we assessed the relationship between repeatability, condition-dependence, attractiveness, age-dependence and viability indicator value of sexual traits using sexual signals as the units of analyses. Those traits that showed high within-year repeatability also showed high between-year repeatability, indicating that between-individual variation is consistent within and among seasons. In addition, age-dependence of traits, probably causing between-year variation, was negatively related to between-year repeatability. Condition-dependence was negatively correlated with effect sizes for the extent to which traits predicted viability. Therefore, traits that are positively related to immediate condition are those that are negatively related to survival, which may be the signature of a trade-off between current and future reproductive success ultimately reflecting signal reliability. No other significant relationship was found between trait attributes. We conclude that multiple sexual signals reflect different aspects of male quality in the barn swallow.     

Sexual differences in larval life history traits of acanthocephalan cystacanths

Sexual differences in life history traits, such as size dimorphism, presumably arise via sexual selection and are most readily observed in adults. For complex life-cycle parasites, however, sexual selection may also have consequences for larval traits, e.g., growth in intermediate hosts. Two acanthocephalan species (Acanthocephalus lucii and Echinorhynchus borealis) were studied to determine, whether larval life histories differ between males and females. The size of female A. lucii cystacanths had a much stronger relationship with intermediate host size than males, suggesting females invest more in growth and are consequently more limited by resources. No relationship between host size and cystacanth size was observed for E. borealis. For both species, female cystacanths survived longer in a culture medium composed entirely of salts, which could suggest that females have greater energy reserves than males. A comparative analysis across acanthocephalan species indicated that sexual size dimorphism at the adult stage correlates with cystacanth dimorphism. However, the relationship was not isometric; cystacanths do not reach the same level of sexual dimorphism as adults, possibly due to resource constraints. Our results suggest that larval life histories diverge between males and females in some acanthocephalans, and this is seemingly a consequence of sexual selection acting on adults.