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In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored.

 

Parental care, mating dynamics and life history co‐evolve. Understanding the diversity of reproductive patterns found in nature is a major focus of evolutionary ecology research. Previous research suggests that the origin of parental care of eggs will be favoured when egg and adult death rates and juvenile survival are relatively high. However, the previous research that explored the link between care and life history did not account for among‐species variation in mating dynamics. As mating dynamics are generally expected to influence care, we explore, theoretically, the life‐history conditions (stage‐specific rates of maturation and survival) that favour parental care across three mating scenarios: reproductive rate (1) is unaffected by males (assuming that some males are present), (2) increases as male abundance increases or (3) decreases as male abundance increases. Across scenarios, all forms of care were most strongly favoured when egg and adult death rates, juvenile survival and female egg maturation rates were relatively high. When reproductive rate was unaffected by male abundance or increased as male abundance increased, as we might expect in systems in which females are mate‐limited, all forms of care were most strongly favoured when male egg maturation rate (i.e. the rate at which male eggs develop, mature and hatch) was moderate or high. When greater male abundance inhibited reproduction, which might occur in systems with intense male–male competition, all forms of care were most strongly favoured when male egg maturation rate was low‐to‐moderate. These results suggest that life history affects the evolution of parental care, and sex‐specific life history can interact with mating dynamics to influence the origin of care.

 

Size‐based harvest limits or gear regulations are often used to manage fishing mortality and ensure the spawning biomass of females is sufficiently protected. Yet, management interactions with species’ mating systems that affect fishery sustainability and yield are rarely considered. For species with obligate male care, it is possible that size‐specific harvest of males will decrease larval production. In order to examine how size‐based management practices interact with mating systems, we modelled fisheries of two species with obligate care of nests, corkwing wrasse (Symphodus melops, Labridae) and lingcod (Ophiodon elongatus,Hexigrammidae) under two management scenarios, a minimum size limit and a harvest slot limit. We simulated the population dynamics, larval production and yield to the fishery under a range of fishing mortalities. We also modelled size‐dependent male care to determine its interaction with management. In both species, the slot limit decreased yield by <12% (relative to minimum size limits) at low fishing mortalities; at higher mortalities, individuals rarely survived to outgrow the slot and spawning potential decreased substantially relative to unfished levels, similar to minimum size limits. Spawning potential decreased less when managed with a slot limit if we included a positive feedback between male size, care and hatching success, but the benefit of implementing the slot depended both on the relative proportions of each sex selected by the fishery and on our assumptions regarding male size and care. This work highlights that the effects of size‐ and sex‐selective fisheries management can be nuanced and produce counter‐intuitive results.

 

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.

 

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.

 

Sexual selection is a powerful force shaping not only the details but also the breadth of what we see in nature. Yet so much unexplained variation remains. Organisms often solve the “problem” of how to pass on their genes in ways that do not fit our current expectations. I argue here that integrating empirical surprises will push our understanding of sexual selection forward. Such “nonmodel” organisms (i.e., species that do not do what we think they should do) challenge us to think deeply, integrate puzzling results, question our assumptions, and consider the new (and arguably better) questions these unexpected patterns pose. In this article, I share how puzzling observations from my long-term research on the ocellated wrasse (Symphodus ocellatus) have shaped my understanding of sexual selection and suggested new questions about the interplay among sexual selection, plasticity, and social interactions. My general premise, however, is not that others should study these questions. Instead, I argue for a change in the culture of our field—to consider unexpected results a welcome opportunity to generate new questions and learn new things about sexual selection. Those of us in positions of power (e.g., as editors, reviewers, and authors) need to lead the way. 

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.