Across taxa, sexually selected traits are more variable in the target sex than 1) the same trait in the opposite sex or 2) non-sexually selected traits, likely due to their condition-dependent expression. In humans, males show greater variability in certain cognitive abilities and brain structures that 1) may facilitate intra- or intersexual competition and 2) are greater/larger in males on average, suggesting these traits may also have been subject to sexual selection. This study investigates sex differences in brain structure variability in chimpanzees. Although male chimpanzees exhibit strong intrasexual competition, reproductive skew is reduced by female mate choice and male coercion. In vivo MRI scans were collected from 226 (135F/91M) individuals and surface areas were calculated for 25 cortical sulci. Outliers for each sex and sulcus were removed prior to analysis. We measured sex differences in variability by calculating the ratio of male-to-female standard deviations of MCMCglmm residuals, controlling for age, rearing condition, scanner type, and kinship. We tested for significant sex differences through permutation. We find that males are significantly more variable at the cingulate (ratio=1.18;p=0.043), middle-frontal (ratio=1.36;p=0.001), occipital-lateral (ratio=1.20;p=0.029), occipital- temporal-marginal (ratio=1.8;p=0.006), superior-temporal (ratio=1.36;p<0.001), subcentral-posterior (ratio=1.62;p=0.033), and superior-parietal (ratio=1.21;p=0.028) sulci. These regions are associated with social perception, face recognition, and motion prediction. Females are more variable at the medio-parietal-occipital sulcus (ratio=0.78;p=0.009), a region associated with planning. This is the first study to demonstrate greater male variability in brain structure in a nonhuman primate species, and suggests sexual selection may lead to greater variability in male cognition across taxa.
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Black and orange coloration predict success during male–male competition in the guppy
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- Award ID(s):
- 1740466
- NSF-PAR ID:
- 10373067
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Behavioral Ecology
- Volume:
- 33
- Issue:
- 6
- ISSN:
- 1045-2249
- Format(s):
- Medium: X Size: p. 1196-1206
- Size(s):
- ["p. 1196-1206"]
- Sponsoring Org:
- National Science Foundation
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Abstract Elaborate, sexually dimorphic traits are widely thought to evolve under sexual selection through female preference, male–male competition, or both. The orangethroat darter (
Etheostoma spectabile ) is a sexually dichromatic fish in which females exhibit no preferences for male size or coloration. We tested whether these traits affect individual reproductive success inE. spectabile when multiple males are allowed to freely compete for a female. The quality and quantity of male coloration were associated with greater success in maintaining access to the female and in spawning as the primary male (first male to participate). On the other hand, sneaking behavior showed little correlation with coloration. Male breeding coloration inE. spectabile may therefore demonstrate how intrasexual competition can be a predominant factor underlying the evolution of male ornaments. -
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Abstract Human activities are altering natural ecosystems, leading to widespread environmental change that can vary across spatiotemporal scales, thus creating dynamic, novel conditions at both large and small scales. In highly disturbed aquatic systems, elevated turbidity is one common stressor that alters the sensory environment of fishes and can disrupt communication, including mate choice, driving population‐level shifts in visual communication traits such as nuptial coloration. At a smaller, within‐population scale, we can expect similar adaptive divergence to a heterogeneous visual landscape. Using the cichlid fish,
Pseudocrenilabrus multicolor, we investigated within‐population variation in diet and nuptial coloration by sampling fish from microhabitats within a relatively small site (~0.14 km2). These visual microhabitats are affected by different types of human disturbance at a very small scale leading to significant differences in water clarity (i.e. turbidity). We used three, non‐mutually exclusive working hypotheses to test if (1) males in low turbidity invest more in carotenoid‐based coloration (economy of pigments hypothesis), (2) fish from low‐turbidity sites eat more carotenoid‐rich foods (diet hypothesis), and (3) fish are habitat matching. Stomach content analyses revealed relatively high overlap in diet across microhabitats; however, fish from stations with the lowest turbidity consumed relatively more plant material (high in carotenoid content) than fish captured at high‐turbidity stations. Males from clearer waters displayed significantly more carotenoid‐based, red and yellow coloration than fish found in microhabitats with higher turbidity, similar to between‐population color variation in this species. Furthermore, larger fish displayed more carotenoid coloration overall, but there was no difference in mean male size among microhabitats suggesting that fish were not sorting into microhabitats. Our results suggest that within‐population variation in nuptial coloration could be associated with microhabitat heterogeneity in the visual landscape driven by turbidity, a diet with more carotenoid‐rich prey items, or a combination of both. -
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Abstract How genetic variation is maintained in ecologically important traits is a central question in evolutionary biology. Male Trinidadian guppies, Poecilia reticulata, exhibit high genetic diversity in color patterns within populations, and field and laboratory studies implicate negative frequency-dependent selection in maintaining this variation. However, behavioral and ecological processes that mediate this selection in natural populations are poorly understood. We evaluated female mate preference in 11 natural guppy populations, including paired populations from high- and low-predation habitats, to determine if this behavior is responsible for negative frequency-dependent selection and to evaluate its prevalence in nature. Females directed significantly more attention to males with rare and unfamiliar color patterns than to males with common patterns. Female attention also increased with the area of male orange coloration, but this preference was independent of the preference for rare and unfamiliar patterns. We also found an overall effect of predation regime; females from high-predation populations directed more attention toward males than those from low-predation populations. Again, however, the habitat-linked preference was statistically independent from the preference for rare and unfamiliar patterns. Because previous research indicates that female attention to males predicts male mating success, we conclude that the prevalence of female preference for males with rare and unfamiliar color patterns across many natural populations supports the hypothesis that female preference is an important process underlying the maintenance of high genetic variation in guppy color patterns.
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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
