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1. Olfactory perception of mates in ecologically divergent stickleback: population parallels and differences

   Mobley, Robert B.; Tillotson, Marquita L.; Boughman, Janette W. (January 2016, Evolutionary ecology research)

   Background: The independent evolution of sympatric species pairs of threespine sticklebacks has provided a natural system to explore how divergent ecologies shape mating preferences. Research has shown that both limnetic and benthic females discriminate against heterospecific males, but not against populations of the same species from different lakes, at least when visual cues are available (Rundle et al., 2000). It is known that olfaction is used in species dis- crimination by benthic but not limnetic sticklebacks in one of the species pairs (Rafferty and Boughman, 2006), but differences across populations are unknown. Hypotheses: Females from benthic habitats make use of olfactory cues to distinguish between species but not lakes of potential mates. Limnetic females will not show preferences for males of different species or lakes when limited to only olfactory cues. Organisms: Benthic and limnetic populations of threespine stickleback (Gasterosteus aculeatus) from Paxton and Priest Lakes, British Columbia. Methods: We exposed gravid females from each population to chemical stimuli from nesting males in a Y-maze, and recorded which stimulus a female chose and how much time was taken to make a decision. Results: We did not find significant differences between female populations in the preference for conspecific over heterospecific male odours. There was also no preference for odours of males from the same or a different lake. In all populations of females, the preference for male odours of different lakes differed between the two species of male odours: benthic male odours from a different lake were selected over limnetic male odours. The amount of time taken to make a decision differed between female populations, but only when benthic females ultimately chose a limnetic male odour over a benthic one. Conclusions: The preference for conspecific over heterospecific odours, although not strong, may still contribute to reproductive isolation in sympatric sticklebacks, particularly through interactions with other senses and environmental properties. 

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2. Little evidence for color- or size-based mating preferences by male strawberry poison frogs (Oophaga pumilio)

   https://doi.org/10.1007/s00265-024-03436-9  

   Lehman, Mik R; González-Santoro, Marco; Richards-Zawacki, Corinne L (February 2024, Behavioral Ecology and Sociobiology)

   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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3. Divergence of chemosensing during the early stages of speciation

   https://doi.org/10.1073/pnas.1921318117  

   van Schooten, Bas; Meléndez-Rosa, Jesyka; Van Belleghem, Steven M.; Jiggins, Chris D.; Tan, John D.; McMillan, W. Owen; Papa, Riccardo (July 2020, Proceedings of the National Academy of Sciences)

   Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries. 

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4. Veiled preferences and cryptic female choice could underlie the origin of novel sexual traits

   https://doi.org/10.1098/rsbl.2018.0878  

   Moehring, Amanda J.; Boughman, Janette W. (February 2019, Biology Letters)

   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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5. Sexual selection and the ascent of women: Mate choice research since Darwin

   https://doi.org/10.1126/science.abi6308  

   Rosenthal, Gil G.; Ryan, Michael J. (January 2022, Science)

   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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