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1. A life-history perspective on sexual selection in a polygamous species

   https://doi.org/10.1186/s12862-020-01618-3  

   Gao, Ke ; van Wijk, Michiel ; Clement, Zoe ; Egas, Martijn ; Groot, Astrid T. ( May 2020 , BMC Evolutionary Biology)

   Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we hypothesize that in polygamous species these roles change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis by assessing fitness costs and benefits of multiple matings in both males and females in a polygamous moth species, as in moths not males but females are the signalers and males are the responders.

   We found that multiple matings confer fitness costs and benefits for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but only 67% of the males and 14% of the females mated successfully in all five nights. In addition, the female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, more than 3 matings decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings.

   Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.

    

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2. Behavioural tactic predicts preoptic-hypothalamic gene expression more strongly than developmental morph in fish with alternative reproductive tactics

   https://doi.org/10.1098/rspb.2017.2742  

   Tripp, Joel A. ; Feng, Ni Y. ; Bass, Andrew H. ( January 2018 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman ( Porichthys notatus ) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioural tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioural tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behaviour. Our results reveal that divergent expression patterns in a conserved neuroendocrine centre known to regulate social-reproductive behaviours across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics. 

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3. Defense against outside competition is linked to cooperation in male–male partnerships

   https://doi.org/10.1093/beheco/arz206  

   Hellmann, Jennifer K. ; Stiver, Kelly A. ; Marsh-Rollo, Susan ; Alonzo, Suzanne H. ; Taborsky, ed., Michael ( December 2019 , Behavioral Ecology)

   Male–male competition is a well-known driver of reproductive success and sexually selected traits in many species. However, in some species, males work together to court females or defend territories against male competitors. Dominant (nesting) males sire most offspring, but subordinate (satellite) males are better able to obtain fertilizations relative to unpartnered males. Because satellites only gain reproductive success by sneaking, there has been much interest in identifying the mechanisms enforcing satellite cooperation (defense) and reducing satellite sneaking. One such potential mechanism is outside competition: unpartnered satellites can destabilize established male partnerships and may force partnered satellites to restrain from cheating to prevent the dominant male from replacing them with an unpartnered satellite. Here, we manipulated perceived competition in the Mediterranean fish Symphodus ocellatus by presenting an “intruding” satellite male to established nesting and satellite male pairs. Focal satellite aggression to the intruder was higher when focal satellites were less cooperative, suggesting that satellites increase aggression to outside competitors when their social position is less stable. In contrast, nesting male aggression to the intruder satellite increased as spawning activity increased, suggesting that nesting males increase their defense toward outside competitors when their current relationship is productive. We found no evidence of altered spawning activity or nesting/satellite male interactions before and after the presentation. These results collectively suggest that response to outside competition is directly linked to behavioral dynamics between unrelated male partners and may be linked to conflict and cooperation in ways that are similar to group-living species.

    

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4. 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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5. Vascularization underlies differences in sexually selected skin coloration in a wild primate

   https://doi.org/10.1111/mec.17026  

   DeLacey, Patricia M. ; Sen, Sharmi ; Schneider‐Crease, India A. ; Chiou, Kenneth L. ; Lemma, Alemayehu ; Ayele, Ferehiwot ; Haile, Abebaw Azanaw ; Lu, Amy ; Bergman, Thore J. ; Beehner, Jacinta C. ; et al ( May 2023 , Molecular Ecology)

   Male reproductive competition can select for condition‐dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male's current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate the mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analysed photographs collected during natural (n = 144) and anaesthetized conditions (n = 38) to understand variability in male and female chest redness, and we used chest skin biopsies (n = 38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within‐individual range in redness under natural conditions. These sex differences were also reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patterns between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or oestrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high‐altitude environment of geladas.

    

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