BACKGROUND Charles Darwin’s Descent of Man, and Selection in Relation to Sex tackled the two main controversies arising from the Origin of Species: the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCE
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Complex sexual-social environments produce high boldness and low aggression behavioral syndromes
Introduction Evidence of animal personality and behavioral syndromes is widespread across animals, yet the development of these traits remains poorly understood. Previous research has shown that exposure to predators, heterospecifics, and urbanized environments can influence personality and behavioral syndromes. Yet, to date, the influence of early social experiences with conspecifics on the development of adult behavioral traits is far less known. We use swordtail fish ( Xiphophorus nigrensis ), a species with three genetically-determined male mating strategies (courtship display, coercion, or mixed strategy) to assess how different early-life social experiences shape adult behavioral development. Methods We raised female swordtails from birth to adulthood in density-controlled sexual-social treatments that varied in the presence of the type of male mating tactics (coercers only, displayers only, coercers and displayers, and mixed-strategists only). At adulthood, we tested females’ boldness, shyness, aggression, sociality, and activity. Results We found that the number of different mating strategies females were raised with (social complexity) shaped behavioral development more than any individual mating strategy. Females reared in complex environments with two male mating tactics were bolder, less shy, and less aggressive than females reared with a single male mating tactic (either courtship only or coercion only). Complex sexual-social environments produced females with behavioral syndromes (correlations between aggression and activity, shyness and aggression, and social interaction and activity), whereas simple environments did not. Discussion Importantly, the characteristics of these socially-induced behavioral syndromes differ from those driven by predation, but converge on characteristics emerging from animals found in urban environments. Our findings suggest that complexity of the sexual-social environment shapes the development of personality and behavioral syndromes to facilitate social information gathering. Furthermore, our research highlights the previously overlooked influence of sexual selection as a significant contributing factor to diverse behavioral development.
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- Award ID(s):
- 1911826
- NSF-PAR ID:
- 10408505
- Date Published:
- Journal Name:
- Frontiers in Ecology and Evolution
- Volume:
- 10
- ISSN:
- 2296-701X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross‐sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long‐term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra,
Pongo abelii ) and Tuanan (Borneo,Pongo pygmaeus wurmbii ), to assess male mating tactics cross‐sectionally in relation to population, male morph (unflanged and flanged), and other socio‐ecological factors. Both our longitudinal and cross‐sectional results confirm and refine previous cross‐sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade‐off between avoiding male‐male contest competition and gaining mating access to females, and thus follow a “best‐of‐a‐bad‐job” mating strategy. -
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Abstract The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (
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Abstract Objectives Chimpanzees (
Pan troglodytes ) are notable for exhibiting high levels of male‐to‐female aggression. Much of this aggression from adult males serves sexually coercive functions. Despite being smaller and lower‐ranking than adult males, adolescent males also engage in regular aggression against adult females. Here, we test whether the primary function of this aggression is sexual coercion, as in adult males, or, alternatively, whether adolescent males use aggression to establish social dominance over females.Materials and Methods We analyzed 1771 copulations and 1812 instances of male‐initiated aggression between adolescent males (aged nine through 14 years) and adult females across 21 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda.
Results Our test of the sexual coercion hypothesis revealed that adolescent males did not selectively target cycling females for aggression, nor did aggression against cycling females predict rates of copulation with those females. Our test of the social dominance hypothesis showed that males succeeded in dominating all adult females before, or soon after, dominating their first adult male. Additionally, we found that adolescent males dominated females approximately in the order of the females' own ranks, from the bottom to the top of the female hierarchy.
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Abstract Animals often communicate in complex, heterogeneous environments, leading to hypothesized selection for increased detectability or discriminability in signaling traits. The extent to which secondary sexual ornaments have evolved to overcome the challenges of signaling in complex environments, however, remains understudied, especially in comparison to their role as indicator traits. This study tested the hypothesis that the condition-dependent secondary sexual ornamentation in the wolf spider Rabidosa rabida functions to increase detectability/discriminability in visually complex environments. We predicted that male ornamentation would interact with the complexity of the signaling environment to affect male mating success. In particular, we expected ornaments to confer a greater mating advantage when males courted in visually complex environments. To test this, we artificially manipulated male foreleg ornamentation (present/absent) and ran repeated-measures mating trials across laboratory microcosms that represented simple versus complex visual signaling environments. Microcosm visual complexity differed in their background pattern, grass stem color, and grass stem placement. We found that ornamented males mated more often and more quickly than unornamented males across both environments, but we found no support for an ornament-by-environment interaction. Male courtship rate, however, did interact with the signaling environment. Despite achieving the same level of mating success across signaling environments, ornamented males courted less rapidly in complex versus simple environments, although environmental complexity had no influence on unornamented male courtship rates. Our results suggest that the visual complexity of the signaling environment influences the interactive influence of ornamentation and dynamic visual courtship on female mate choice.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fevo.2022.1050569
