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Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as ‘veiled preferences’ that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference.
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Little evidence for color- or size-based mating preferences by male strawberry poison frogs (Oophaga pumilio)
AbstractWhile there are many studies documenting female mating preferences across taxa, male mate choice remains relatively understudied. Male mate choice often develops when there is variation in female quality and thus the fitness benefits of mating with particular females. Specifically, males tend to prefer females with traits that confer direct fitness benefits such as large body size, which may be linked with high fecundity. Prior work has shown that females of the strawberry poison frog,Oophaga pumilio, prefer males bearing certain coloration (most often the female’s own color), and that this preference can be learned through maternal imprinting. Females have been shown to prefer larger males as well. Here we test whether similar mate preferences for color and size exist in males of this species using two-way choice tests on captive bred maleO. pumilio. In each test focal males were placed in an arena with two stimulus females: either both of the same size but differing in color, or both of the same color but differing in size. We found only weak evidence for behavioral biases toward particular colors and no evidence for biases toward larger females, suggesting that males ofO. pumiliodo not predictably choose mates based on these female traits. Despite several aspects of their natural history that suggest males have reasons to be choosy, our findings suggest that the cost of mate rejection may outweigh any fitness benefits derived from being selective of mates. Studies of additional populations, ideally conducted on wild individuals, are needed to better understand the range of conditions under which males may exhibit mate choice and the types of traits on which they base these choices. Significance statementTo fully understand the fitness landscapes and evolutionary trajectories that result from sexual selection, we need to understand when and how the mate preferences of the two sexes act and interact. While female mate choice has been widely studied, male mate choice remains poorly understood. To help bridge this gap, we studied male mate preferences in the strawberry poison frogOophaga pumilio, a small brightly colored frog for which female preferences for male color and size have been well-documented. We found no evidence that maleO. pumilioexhibit mate preferences based on female size and little evidence for male mate preferences based on female color. This is surprising given that larger females are often more fecund, maleO. pumilioare known to exhibit color-based behavioral biases in the context of male-male competition, and both sexes provide parental care.
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- Award ID(s):
- 2050358
- PAR ID:
- 10573249
- Publisher / Repository:
- Springer
- Date Published:
- Journal Name:
- Behavioral Ecology and Sociobiology
- Volume:
- 78
- Issue:
- 2
- ISSN:
- 0340-5443
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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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. 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Abstract Investigating how intrasexual competition and intersexual mate choice act within a system is crucial to understanding the maintenance and diversity of sexually-dimorphic traits. These two processes can act in concert by selecting for the same trait, or in opposition by selecting for different extremes of the same trait; they can also act on different traits, potentially increasing trait complexity. We asked whether male–male competition and female mate choice act on the same male traits using Trinidadian guppies, which exhibit sexual size dimorphism and male-limited color patterns consisting of different colors arranged along the body and fins. We used behavioral assays to assess the relationship between color and competitive success and then compared our results to the plethora of data on female choice and color in our study population. Males initiated more contests if they were larger than their competitor. Males won contests more often if they had more black coloration than their competitor, and the effect of black was stronger when males had less orange than their competitor. Additionally, males won more often if they had either more structural color (iridescence) and more orange, or less structural color and less orange than their competitor, suggesting multiple combinations of color traits predict success. Females from our study population exhibit a strong preference for more orange coloration. Thus, traits favored in male contests differ from those favored by intersexual selection in this population. These results suggest that inter- and intrasexual selection, when acting concurrently, can promote increased complexity of sexually selected traits.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1007/s00265-024-03436-9
