Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems

The hypothesis that epigenetic mechanisms of gene expression regulation have two main roles in vertebrate sex is presented. First, and within a given generation, by contributing to the acquisition and maintenance of (i) the male or female function once during the lifetime in individuals of gonochoristic species; and (ii) the male and female function in the same individual, either at the same time in simultaneous hermaphrodites, or first as one sex and then as the other in sequential hermaphrodites. Second, if environmental conditions change, epigenetic mechanisms may have also a role across generations, by providing the necessary phenotypic plasticity to facilitate the transition: (i) from one sexual system to another, or (ii) from one sex-determining mechanism to another. Furthermore, if the environmental change lasts enough time, epimutations could facilitate assimilation into genetic changes that stabilize the new sexual system or sex-determining mechanism. Examples supporting these assertions are presented, caveats or difficulties and knowledge gaps identified, and possible ways to test this hypothesis suggested. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

Male mate choice unresolved in the mangrove rivulus

Mate choice has the potential to drive phenotypic evolution because it can determine traits that increase an individual’s likelihood to reproduce (courtship behaviors, elaborate ornamentation). These traits, however, can also be detrimental for health or survival, often antagonizing the evolution of extreme phenotypes. Mangrove rivulus fish (Kryptolebias marmoratus) develop as self-fertilizing simultaneous hermaphrodites. Hermaphrodites overwhelmingly self-fertilize their eggs internally, but occasionally oviposit unfertilized eggs. Some individuals change sex to male after sexual maturity, essentially forgoing the reproductive assurance of selfing. In a continuing effort to understand how sex change to male is maintained this species, I designed an experiment to determine whether males act as choosers to increase their likelihood of finding unfertilized eggs for reproduction. I hypothesized that males would prefer to associate with younger hermaphrodites when given a dichotomous choice, as they lay a greater proportion of unfertilized eggs compared to older hermaphrodites. The males in this study did not show a preference for either the younger or older hermaphrodite but exhibited greater within individual variance across subtrials than among individual variation. I discuss alternative hypotheses concerning male mate choice in mangrove rivulus, which may illuminate hypotheses to be tested in this and other hermaphroditic species.

How do whale barnacles live on their hosts? Functional morphology and mating-group sizes of Coronula diadema (Linnaeus, 1767) and Conchoderma auritum (Linnaeus, 1767) (Cirripedia: Thoracicalcarea)

Whale-associated barnacles are intriguing in terms of their planktonic food sources, mating habits, and mechanisms of host attachment. We present observations of the whale-associated barnacles Coronula diadema (Linnaeus, 1767) and Conchoderma auritum (Linnaeus, 1767) obtained from dead humpback whales (Megaptera novaeangliae (Borowski, 1781)) collected in Korea. Shell bases of Coronula diadema are inflected and sharp-edged with hollow coring tubes at the periphery. The coring tubes are filled with whale skin, supporting the model that shell accretion into the whale skin is achieved by basal constriction to achieve strong attachment. Conchoderma auritum attaches to the shell surfaces of Coronula and has a pair of tubular ear-shaped structures on the capitulum. Both species have short and thick-segmented cirri that allow feeding in strong currents. The distal ends of the cirri in both species are often equipped with sharp, large claw-like setae, which are likely used to capture large zooplankton for food. Coronula diadema and Conchoderma auritum are simultaneous hermaphrodites. Coronula diadema can mate up to nine surrounding individuals. Conchoderma auritum lives in clumps and mating group size can up to 26 individuals.

An Evolutionary Ecological Approach to Sex Allocation and Sex Determination in Crustaceans

This chapter reviews sex determination and sex allocation strategies among crustaceans with different sexual systems (gonochorism, sequential and simultaneous hermaphroditism, and androdioecy), from the perspective of evolutionary ecology. The discussion includes genetic, environmental, and cytoplasmic sex determination in free-living and parasitic crustaceans, timing and frequency of sex change especially in partial protandry, the effects of mating group size on resource allocation by simultaneous hermaphrodites, and sex ratio and determination in androdioecious crustaceans. The fascinating diversity of crustacean reproduction stimulated theoretical biologists to construct models to explain them, and empirical biologists attempted to test hypotheses derived from those models. This review clearly shows that the interaction between theoretical and empirical studies has facilitated understanding of the evolutionary conditions of diverse sexual strategies among crustaceans. Since sexual strategies often interact with other aspects of adaptive strategies such as life history, integrating different aspects into both theoretical and empirical studies will provide further understandings into crustacean sexual systems. In addition, the authors point out the potential of phylogenetic comparative analyses using natural history data as a tool to understand the tempo and mode of evolution of sex allocation strategies.

Evolution of sex allocation plasticity and its predictors in a flatworm genus

Local sperm competition (LSC), which occurs when related sperm compete for access to a given set of eggs, can influence sex allocation (SA) in simultaneous hermaphrodites. Different factors that have been predicted to affect LSC—and hence, optimal SA—include the mating strategy (such as reciprocal mating vs. hypodermic insemination) and the ability to self-fertilize. Moreover, the level of LSC experienced could vary temporally and/or spatially, favouring the evolution of SA plasticity. However, it is unknown how the mating strategy and ability to self-fertilize can influence SA and SA plasticity. Here, we explored this by collecting estimates of SA and SA plasticity for seven species of the flatworm genus, Macrostomum, and performing analyses while controlling for phylogeny. While we found substantial interspecific variation in SA, neither the mating strategy nor the ability to self-fertilize had a significant effect on SA. Next, we estimated standardized effect sizes for SA plasticity in response to i) the presence of mating partners and ii) the strength of LSC for each species, and tested if the mating strategy or ability to self-fertilize predicted these effect sizes. We found considerable interspecific variation in SA plasticity, with some species being highly plastic and others showing no significant plasticity. Moreover, self-fertilization predicted SA plasticity with respect to the presence of mating partners, with SA plasticity being lower for self-fertilizing species. Finally, we showed that interspecific variation in SA is nearly three times higher than intraspecific variation, suggesting that SA estimates in field-collected specimens can, at least to some degree, be interpreted as representing interspecific rather than intraspecific variation. Our study suggests that both SA and SA plasticity can evolve rapidly, with self-fertilization being an important predictor for the latter in Macrostomum.

Experience and relatedness influence mating interactions in a simultaneously hermaphroditic snail, Physa gyrina

The means by which animals assess potential mates is an important issue in studies of reproductive systems. I tested whether an individual’s previous experiences and the relatedness of mates affected mating behavior in a simultaneous hermaphrodite snail, Physa gyrina. Previous work with this species showed reduced reproductive success resulting from both strong outbreeding and inbreeding. Thus, I predicted that individuals should prefer partners of intermediate relatedness. During activity trials, snails moved longer distances when exposed to chemical cues from conspecifics of lesser relatedness. Furthermore, during mating interactions, behavioral responses to relatedness varied with gender-role: male-role behaviors did not vary across relatedness treatments, while snails paired with either closely related or highly dissimilar partners increased their female-role resistance behaviors as interactions escalated. Experiences with their current partner also affected behavioral dynamics. Familiar pairs had fewer matings and longer latency times until a mating occurred than unfamiliar pairs. Snails acting in the female role also exhibited higher resistance rates in familiar pairs than in unfamiliar pairs. Previous, brief exposure to chemical cues in a non-mating context also influenced behavior during a subsequent mating interaction. Snails that were previously exposed to chemical cues from unfamiliar individuals tended to be more likely to occupy the male role following an encounter, and had significantly lower copulation frequencies and higher female-role resistance rates (i.e. were choosier) than those previously exposed to cues from familiar individuals. Overall, the results show that: 1) relatedness, past exposure to conspecific chemical cues, and experience with a current partner all influence mating behaviors in these snails; and 2) in these simultaneous hermaphrodites, an individual’s responses depend on whether it is occupying the male or female role.

The evolution of egg trading in simultaneous hermaphrodites

Egg trading, whereby simultaneous hermaphrodites exchange each other’s eggs for fertilization, constitutes one of the few rigorously documented and most widely cited examples of direct reciprocity among unrelated individuals. Yet how egg trading may initially invade a population of non-trading simultaneous hermaphrodites is still unresolved. Here, we address this question with an analytical model that considers mate encounter rates and costs of egg production in a population that may include traders (who provide eggs for fertilization only if their partners also have eggs to reciprocate), providers (who provide eggs regardless of whether their partners have eggs to reciprocate), and withholders (“cheaters” who only mate in the male role and just use their eggs to elicit egg release from traders). Our results indicate that a combination of inter-mediate mate encounter rates, sufficiently high costs of egg production, and a sufficiently high probability that traders detect withholders (in which case eggs are not provided) is conducive to the evolution of egg trading. Under these conditions traders can invade—and resist invasion from—providers and withholders alike. The prediction that egg trading evolves only under these specific conditions is consistent with the rare occurrence of this mating system among simultaneous hermaphrodites.