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1. Sperm and alternative reproductive tactics: a review of existing theory and empirical data

   https://doi.org/10.1098/rstb.2020.0075  

   Kustra, Matthew C. ; Alonzo, Suzanne H. ( December 2020 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   null (Ed.)

   Males that exhibit alternative reproductive tactics (ARTs) often differ in the risk of sperm competition and the energetic trade-offs they experience. The resulting patterns of selection could lead to between-tactic differences in ejaculate traits. Despite extensive research on male ARTs, there is no comprehensive review of whether and what differences in sperm traits exist between male ARTs. We review existing theory on ejaculate evolution relevant to ARTs and then conduct a comprehensive vote-counting review of the empirical data comparing sperm traits between males adopting ARTs. Despite the general expectation that sneaker males should produce sperm that are more competitive (e.g. higher quality or performance), we find that existing theory does not predict explicitly how males adopting ARTs should differ in sperm traits. The majority of studies find no significant difference in sperm performance traits between dominant and sneaker males. However, when there is a difference, sneaker males tend to have higher sperm performance trait values than dominant males. We propose ways that future theoretical and empirical research can improve our understanding of the evolution of ejaculate traits in ARTs. We then highlight how studying ejaculate traits in species with ARTs will improve our broader knowledge of ejaculate evolution. This article is part of the theme issue ‘Fifty years of sperm competition’. 

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2. Genital morphology associated with mating strategy in the polymorphic lizard, Uta stansburiana

   https://doi.org/10.1002/jmor.20930  

   Gilman, Casey A. ; Corl, Ammon ; Sinervo, Barry ; Irschick, Duncan J. ( December 2018 , Journal of Morphology)

   Sexual selection can lead to rapid evolution of sexual traits and striking morphological diversity across taxa. In populations where competition for mates is intense, males sometimes evolve distinct behavioral strategies along with morphological differences that help them secure mating opportunities. Strong postcopulatory selection and differential resource allocation across male strategy type can result in strategy‐specific differences in sexual traits, such as sperm morphology, ejaculate components, and testis size. Some polymorphic species also have strategy‐specific genital morphology. Thus far, among vertebrates, this has only been observed in fish. Here, we present the first morphological description of the intromittant copulatory organ, the hemipenis, of the three mating types of the side‐blotched lizard,Uta stansburiana, from a population that exhibits alternative mating strategies. We found that the isometrically scaling hemipenis was shortest in the nonterritorial (yellow) morph that sneaks copulations with other males' mates. Although the hemipenes were generally the same shape across morphs, the usurping territorial (orange) morph had a significantly wider apical horn than the nonterritorial sneaker morph. Sneaker males also had smaller relative body masses than both the mate‐guarding (blue) morph and the usurper morph, and shorter tibia than the usurper morph. This study using a small sample of males suggests that strong sexual selection may drive genital trait differentiation across morphs within populations of terrestrial vertebrates.

    

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3. Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour, sperm characteristics and social interactions

   https://doi.org/10.1111/mec.14999  

   Nugent, Bridget M. ; Stiver, Kelly A. ; Hofmann, Hans A. ; Alonzo, Suzanne H. ( February 2019 , Molecular Ecology)

   While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.

    

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4. Extreme variation in testes size in an insect is linked to recent mating activity

   https://doi.org/10.1111/jeb.13574  

   Greenway, E. V ; Cirino, Lauren A. ; Wilner, Daniela ; Somjee, Ummat ; Anagnostou, Maria‐Eleni ; Hepple, Russell T. ; Miller, Christine W. ( December 2019 , Journal of Evolutionary Biology)

   Ample sperm production is essential for successful male reproduction in many species. The amount of sperm a male can produce is typically constrained by the size of his testes, which can be energetically expensive to grow and maintain. Although the economics of ejaculate allocation has been the focus of much theoretical and empirical literature, relatively little attention has been paid to individual adult variation and plasticity at the source of sperm production, the testes themselves. We experimentally address this issue using the insectNarnia femorataStål (Hemiptera: Coreidae). We established the metabolic cost of testicular tissue and then quantified variation in individual testes mass in response to multiple mate quality and quantity treatments.We uncovered extreme variation across individuals and considerable short‐term effects of mating activity on testes dry mass. Importantly, the observed variation in testes mass was associated with notable fitness consequences; females paired with males with larger testes had greater hatching success. Overall, pairing with a female resulted in a 11% reduction indrytestes mass. Despite this apparent considerable mating investment, we found no evidence of strategic allocation to higher quality females or longer‐term changes in testes mass. The dynamic nature of testes mass and its metabolic cost is vital to consider in the context of re‐mating rates, polyandry benefits and general mating system dynamics both in this species and more broadly.

    

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5. Cognitive-Behavioral Divergence Is Greater Across Alternative Male Reproductive Phenotypes Than Between the Sexes in a Wild Wrasse

   https://doi.org/10.3389/fevo.2022.929595  

   Cummings, Molly E. ; Marsh-Rollo, Susan E. ; Alonzo, Suzanne H. ( July 2022 , Frontiers in Ecology and Evolution)

   Sexual selection is a powerful diversifier of phenotype, behavior and cognition. Here we compare cognitive-behavioral traits across four reproductive phenotypes (females and three alternative males) of wild-caught ocellated wrasse ( Symphodus ocellatus ). Both sex and alternative male phenotypes are environmentally determined with sex determination occuring within the first year, and males transition between alternative phenotypes across 2 years (sneaker to satellite or satellite to nesting). We captured 151 ocellated wrasse and tested them on different behavior and cognition assays (scototaxis, shoaling, and two detour-reaching tasks). We found greater divergence across alternative male reproductive phenotypes than differences between the sexes in behavior, problem-solving, and relationships between these traits. Nesting males were significantly less bold than others, while sneaker males were faster problem-solvers and the only phenotype to display a cognitive-behavioral syndrome (significant correlation between boldness and problem-solving speed). Combining these results with prior measurements of sex steroid and stress hormone across males, suggests that nesting and sneaker males represent different coping styles. Our data suggests that transitioning between alternative male phenotypes requires more than changes in physiology (size and ornamentation) and mating tactic (sneaking vs. cooperation), but also involves significant shifts in cognitive-behavioral and coping style plasticity. 

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