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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. 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)

   Abstract 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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3. 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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4. Cryptic Mate Preference in Male Bicyclus anynana Butterflies

   https://doi.org/10.1007/s10905-023-09814-x  

   Siebenmorgen, Jacob P.; Tibbs, Taryn L.; Robertson, Deonna N.; Westerman, Erica L. (March 2023, Journal of Insect Behavior)

   While male mate choice has received sparse attention in comparison to female choice, it occurs often in insects. In addition, male insects may preferentially allocate sperm and ejaculate in response to female quality. Previous research indicates that male Bicyclus anynana butterflies can learn mate preference through prior exposure to females, though naïve males mate randomly. It is unclear whether this preference learning may also influence male sperm and ejaculate allocation after mate selection, or whether males have cryptic mate preference for female wing patterns independent of preference learning. Here we test whether B. anynana males adjust their sperm and ejaculate allocation in response to a learned preference. We also assess whether males exhibit an innate cryptic preference and adjust their sperm and ejaculate in response to female wing pattern. We compared number of eggs laid by females and spermatophore (male butterfly ejaculate) weight in four no-choice treatments: naïve male butterflies (having no prior exposure to females), paired with a 2 or 0-spot female, and experienced male butterflies (having a previous three-hour interaction with a 0-spot female), paired with a 2 or 0-spot female. All females used were naturally 2-spot females, 0-spot females had artificially blocked spots. We found that 0-spot females laid significantly more eggs than 2-spot females, independent of male experience. There was no effect of female phenotype or male experience on spermatophore weight. Our findings suggest that male B. anynana have an innate cryptic preference for 0-spot females, which has been shown in other studies to only be seen as a pre-copulatory preference when enhanced by early experience. 

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5. 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)

   Abstract 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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