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.
more »
« less
Cognitive-Behavioral Divergence Is Greater Across Alternative Male Reproductive Phenotypes Than Between the Sexes in a Wild Wrasse
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.
more »
« less
- NSF-PAR ID:
- 10386628
- Date Published:
- Journal Name:
- Frontiers in Ecology and Evolution
- Volume:
- 10
- ISSN:
- 2296-701X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
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. -
Across taxa, sexually selected traits are more variable in the target sex than 1) the same trait in the opposite sex or 2) non-sexually selected traits, likely due to their condition-dependent expression. In humans, males show greater variability in certain cognitive abilities and brain structures that 1) may facilitate intra- or intersexual competition and 2) are greater/larger in males on average, suggesting these traits may also have been subject to sexual selection. This study investigates sex differences in brain structure variability in chimpanzees. Although male chimpanzees exhibit strong intrasexual competition, reproductive skew is reduced by female mate choice and male coercion. In vivo MRI scans were collected from 226 (135F/91M) individuals and surface areas were calculated for 25 cortical sulci. Outliers for each sex and sulcus were removed prior to analysis. We measured sex differences in variability by calculating the ratio of male-to-female standard deviations of MCMCglmm residuals, controlling for age, rearing condition, scanner type, and kinship. We tested for significant sex differences through permutation. We find that males are significantly more variable at the cingulate (ratio=1.18;p=0.043), middle-frontal (ratio=1.36;p=0.001), occipital-lateral (ratio=1.20;p=0.029), occipital- temporal-marginal (ratio=1.8;p=0.006), superior-temporal (ratio=1.36;p<0.001), subcentral-posterior (ratio=1.62;p=0.033), and superior-parietal (ratio=1.21;p=0.028) sulci. These regions are associated with social perception, face recognition, and motion prediction. Females are more variable at the medio-parietal-occipital sulcus (ratio=0.78;p=0.009), a region associated with planning. This is the first study to demonstrate greater male variability in brain structure in a nonhuman primate species, and suggests sexual selection may lead to greater variability in male cognition across taxa.more » « less
-
more » « less
Abstract Many species have evolved alternate phenotypes, thus enabling individuals to conditionally produce phenotypes that are favorable for reproductive success. Examples of this phenomenon include sexual dimorphism, alternative reproductive strategies, and social insect castes. While the evolutionary functions and developmental mechanisms of dimorphic phenotypes have been studied extensively, little attention has focused on the evolutionary covariance between each phenotype. We extend the conceptual framework and methods of morphological integration to hypothesize that dimorphic traits tend to be less integrated between sexes or social castes. In the case of social insects, we describe results from our recent study of an ant genus in which workers have major and minor worker castes that perform different behavioral repertoires in and around the nest. In the case of birds, we describe a new analysis of a family of songbirds that exhibits plumage coloration that can differ greatly between males and females, with apparently independent changes in each sex. Ant head shape, which is highly specialized in each worker caste, was weakly integrated between worker castes, whereas thorax shape, which is more monomorphic, was tightly integrated. Similarly, in birds, we found a negative association between dimorphism and the degree of integration between sexes. We also found that integration decreased in fairy wrens (Malurus) for many feather patches that evolved greater dichromatism. Together, this suggests that the process of evolving increased dimorphism results in a decrease in integration between sexes and social castes. We speculate that once a mechanism for dimorphism evolves, that mechanism can create independent variation in one sex or caste upon which selection may act.
-
more » « less
Abstract Estrogenic signaling is an important focus in studies of gonadal and brain sexual differentiation in fishes and vertebrates generally. This study examined variation in estrogenic signaling (1) across three sexual phenotypes (female, female‐mimic initial phase [IP] male, and terminal phase [TP] male), (2) during socially‐controlled female‐to‐male sex change, and (3) during tidally‐driven spawning cycles in the protogynous bluehead wrasse (
Thalassoma bifasciatum ). We analyzed relative abundances of messenger RNAs (mRNAs) for the brain form of aromatase (cyp19a1b ) and the three nuclear estrogen receptors (ER) (ERα, ERβa , andERβb ) by qPCR. Consistent with previous reports, forebrain/midbraincyp19a1b was highest in females, significantly lower in TP males, and lowest in IP males. By contrast,ERα andERβb mRNA abundances were highest in TP males and increased during sex change.ERβa mRNA did not vary significantly. Across the tidally‐driven spawning cycle,cyp19a1b abundances were higher in females than TP males. Interestingly,cyp19a1b levels were higher in TP males close (~1 h) to the daily spawning period when sexual and aggressive behaviors rise than males far from spawning (~10–12 h). Together with earlier findings, our results suggest alterations in neural estrogen signaling are key regulators of socially‐controlled sex change and sexual phenotype differences. Additionally, these patterns suggest TP male‐typical sociosexual behaviors may depend on intermediate rather than low estrogenic signaling. We discuss these results and the possibility that an inverted‐U shaped relationship between neural estrogen and male‐typical behaviors is more common than presently appreciated.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fevo.2022.929595
