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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. 

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only “sneak” spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production. 

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.