Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization
- PAR ID:
- 10461113
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 32
- Issue:
- 6
- ISSN:
- 1010-061X
- Format(s):
- Medium: X Size: p. 545-558
- Size(s):
- p. 545-558
- Sponsoring Org:
- National Science Foundation
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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/ SCIENCEmore » « less
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Patricelli, Gail L. (Ed.)
Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, “Inferred Attractiveness.” In this model, females acquire mating preferences by observing others’ choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling “good genes.” However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.
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null (Ed.)Due to extreme incongruence in parental investment, the potential for sexual conflict in orangutan reproductive strategies is high. Female orangutans prefer flanged males, but with intense male-male competition and sexual coercion, it is unclear how females are able to exert choice. We hypothesized that female orangutans use initiation and maintenance of associations with preferred males as a mechanism of female choice. We used encounter rates and behavioral measures of proximity maintenance to distinguish between the role of female choice and male coercion in male-female associations in Gunung Palung National Park, West Kalimantan, Indonesia. From May 2018-April 2019, we collected data on initiation, termination, and proximity maintenance during associations between males and cycling females (females without dependent offspring or with offspring over 6 years old). Encounters between cycling females and flanged males were more likely to be female-initiated (83.3%), while encounters with unflanged males were more likely to be male-initiated (80%) (N=16, p=0.035, Fisher’s exact test). Additionally, the Brown Index indicates significantly more female proximity maintenance when cycling females associated with flanged males than unflanged males (N=33, W = 198.5, p= 0.012). However, using long-term data on male-female associations, we found that dyads of flanged males and females were less likely to encounter other males compared to dyads of unflanged males and females (N=542, χ2= 3.3051, df=1, p=0.035). This indicates that flanged males may also use associations to mate guard females. These data indicate that there are behavioral manifestations of both female choice and male coercion in orangutan associations. Funders: NSF (DGE-1247312, BCS-1638823, BCS-0936199), Boston University, Leakey Foundation, Disney Conservation Fund, and US Fish and Wildlife Service (F18AP00898)more » « less
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null (Ed.)Due to extreme incongruence in parental investment, the potential for sexual conflict in orangutan reproductive strategies is high. Female orangutans prefer flanged males, but with intense male-male competition and sexual coercion, it is unclear how females are able to exert choice. We hypothesized that female orangutans use initiation and maintenance of associations with preferred males as a mechanism of female choice. We used encounter rates and behavioral measures of proximity maintenance to distinguish between the role of female choice and male coercion in male-female associations in Gunung Palung National Park, West Kalimantan, Indonesia. From May 2018-April 2019, we collected data on initiation, termination, and proximity maintenance during associations between males and cycling females (females without dependent offspring or with offspring over 6 years old). Encounters between cycling females and flanged males were more likely to be female-initiated (83.3%), while encounters with unflanged males were more likely to be male-initiated (80%) (N=16, p=0.035, Fisher’s exact test). Additionally, the Brown Index indicates significantly more female proximity maintenance when cycling females associated with flanged males than unflanged males (N=33, W = 198.5, p= 0.012). However, using long-term data on male-female associations, we found that dyads of flanged males and females were less likely to encounter other males compared to dyads of unflanged males and females (N=542, χ2= 3.3051, df=1, p=0.035). This indicates that flanged males may also use associations to mate guard females. These data indicate that there are behavioral manifestations of both female choice and male coercion in orangutan associations. Funders: NSF (DGE-1247312, BCS-1638823, BCS-0936199), Boston University, Leakey Foundation, Disney Conservation Fund, and US Fish and Wildlife Service (F18AP00898)more » « less
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null (Ed.)Abstract Sexual coercion, in the form of forced copulations, is relatively frequently observed in orangutans and generally attributed to their semi-solitary lifestyle. High ecological costs of association for females may be responsible for this lifestyle and may have prevented the evolution of morphological fertility indicators (e.g., sexual swellings), which would attract (male) associates. Therefore, sexual conflict may arise not only about mating per se but also about associations, because males may benefit from associations with females to monitor their reproductive state and attempt to monopolize their sexual activities. Here, we evaluate association patterns and costs for females when associating with both males and females of two different orangutan species at two study sites: Suaq, Sumatra ( Pongo abelii ), and Tuanan, Borneo ( Pongo pygmaeus wurmbii ). Female association frequency with both males and females was higher in the Sumatran population, living in more productive habitat. Accordingly, we found that the cost of association, in terms of reduced feeding to moving ratio and increased time being active, is higher in the less sociable Bornean population. Males generally initiated and maintained such costly associations with females, and prolonged associations with males led to increased female fecal cortisol metabolite (FCM) levels at Tuanan, the Bornean population. We conclude that male-maintained associations are an expression of sexual conflict in orangutans, at least at Tuanan. For females, this cost of association may be responsible for the lack of sexual signaling, while needing to confuse paternity. Significance statement Socioecological theory predicts a trade-off between the benefits of sociality and the ecological costs of increased feeding competition. Orangutans’ semi-solitary lifestyle has been attributed to the combination of high association costs and low predation risk. Previous work revealed a positive correlation between association frequencies and habitat productivity, but did not measure the costs of association. In this comparative study, we show that females likely incur costs from involuntary, male-maintained associations, especially when they last for several days and particularly in the population characterized by lower association frequencies. Association maintenance therefore qualifies as another expression of sexual conflict in orangutans, and especially prolonged, male-maintained associations may qualify as an indirect form of sexual coercion.more » « less