Nils Anthes

Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework

A key issue in the study of the behaviour of copulating simultaneous hermaphrodites concerns the decision about which sexual role to adopt in a mating encounter. If two mates share a preference to adopt the same sexual role, mating interests are inherently incompatible. We review previous models that have explored the origin of, and resolutions to, such gender conflicts: (1) sex allocation models; (2) risk-averse models; (3) costly male function models; and (4) game-theoretical models. None of these satisfactorily accounts for the diversity found in hermaphrodite mating systems, either because the assumptions of the model reflect lifetime decisions rather than single mating decisions, or because only a narrow set of environmental conditions is considered. Furthermore, some often cited predictions such as a preference for copulating in the female role or a prevalence of conditional sperm exchange (‘sperm trading’) face limited empirical support. To reconcile and extend these previous ideas, we propose the gender ratio hypothesis as a more general model framework. Here, sex role preferences derive from the potential fitness gain per mating event. Preferences can thus vary considerably within and between individuals, but are predicted to be usually male biased. By combining sex role preference with mating rate, our hypothesis can explain the existence of a wide range of hermaphrodite mating systems, including unconditional reciprocity in systems where sperm trading has been predicted but not found.

Bateman Gradients in Hermaphrodites: An Extended Approach to Quantify Sexual Selection

Sexual selection is often quantified using Bateman gradients, which represent sex‐specific regression slopes of reproductive success on mating success and thus describe the expected fitness returns from mating more often. Although the analytical framework for Bateman gradients aimed at covering all sexual systems, empirical studies are biased toward separate‐sex organisms, probably because important characteristics of other systems remain incompletely treated. Our synthesis complements the existing Bateman gradient approach with three essential reproductive features of simultaneous hermaphrodites. First, mating in one sex may affect fitness via the opposite sex, for example, through energetic trade‐offs. We integrate cross‐sex selection effects and show how they help characterizing sexually mutualistic versus antagonistic selection. Second, male and female mating successes may be correlated, complicating the interpretation of Bateman gradients. We show how to quantify the impact of this correlation on sexual selection and propose a principal component analysis on male and female mating success to facilitate interpretation. Third, self‐fertilization is accounted for by adding selfed progeny as a separate category of reproductive success to analyses of Bateman gradients. Finally, using a worked example from the snail Biomphalaria glabrata, we illustrate how the extended analytical framework can enhance our understanding of sexual selection in hermaphroditic animals and plants.

Hermaphrodite sex role preferences : the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.

Functions, diversity, and evolution of traumatic mating

Copulation can involve the wounding of the mating partner by specialised devices. This type of mating, which we term traumatic mating, has been regarded as exceptional. Its prevalence, however, has not been compared across taxa, nor have its functions and putative evolutionary pathways. A categorisation has been lacking to date. We here show that traumatic mating is a widespread and diverse phenomenon that likely evolved via several pathways. Its putative functions include: (i) anchorage during mating; (ii) stimulation of short‐term female reproductive investment; (iii) male paternity advantages; and (iv) enhanced fertilisation efficiency in transitions to internal fertilisation. Both natural and sexual selection have likely contributed to the parallel evolution of traumatic intromittent organs in phylogenetically distant taxa. These organs are sometimes remarkably similar in shape and often, but not always, inject sperm. The target sites of trauma infliction and the nature of secretions delivered alongside sperm are thus far poorly studied, but data on both are needed to elucidate the function of traumatic mating. The few existing studies that explicitly quantify fitness impacts of traumatic mating indicate that this strategy may often be costly to the party being wounded. However, a comprehensive approach to assess overall investments and returns for both sexes is a major target for future work. Finally, for the first time, we corroborate quantitatively the hypothesis that traumatic mating evolved relatively more often among hermaphroditic than among gonochoric taxa.

How does breeding system variation modulate sexual antagonism

The study of sexually antagonistic (SA) traits remains largely limited to dioecious (separate sex), mobile animals. However, the occurrence of sexual conflict is restricted neither by breeding system (the mode of sexual reproduction, e.g. dioecy or hermaphroditism) nor by sessility. Here, we synthesize how variation in breeding system can affect the evolution and expression of intra- and inter-locus sexual conflicts in plants and animals. We predict that, in hermaphrodites, SA traits will (i) display lower levels of polymorphism; (ii) respond more quickly to selection; and (iii) involve unique forms of interlocus conflict over sex allocation, mating roles and selfing rates. Explicit modelling and empirical tests in a broader range of breeding systems are necessary to obtain a general understanding of the evolution of SA traits.

Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug.

Reciprocity constitutes the prevalent mating mechanism among simultaneous hermaphrodites. Yet, when copulations in the female role confer fitness costs through male manipulation, it becomes advantageous sometimes to mate unilaterally in the male role only. In the sea slug Siphopteron quadrispinosum, acting males stab their partner with a bipartite penis, which not only hypodermically injects prostate fluids, but also apparently mechanically enforces unilateral male matings. Despite a pronounced male mating drive in both partners, unilaterality ensued when one slug stabbed more rapidly than its partner. The acting male may thus avoid the costs inflicted by traumatic injections and penial spines. While future studies need to elucidate the net fitness consequences of stabbing, our behavioural evidence is in line with the hypothesis that mating in S. quadrispinosum represents conflicting rather than complementary mating interests between mates.

Darwinian sex roles confirmed across the animal kingdom

Consistent with Darwin’s ideas, this meta-analysis reveals that males experience stronger sexual selection than females. Since Darwin’s conception of sexual selection theory, scientists have struggled to identify the evolutionary forces underlying the pervasive differences between male and female behavior, morphology, and physiology. The Darwin-Bateman paradigm predicts that anisogamy imposes stronger sexual selection on males, which, in turn, drives the evolution of conventional sex roles in terms of female-biased parental care and male-biased sexual dimorphism. Although this paradigm forms the cornerstone of modern sexual selection theory, it still remains untested across the animal tree of life. This lack of evidence has promoted the rise of alternative hypotheses arguing that sex differences are entirely driven by environmental factors or chance. We demonstrate that, across the animal kingdom, sexual selection, as captured by standard Bateman metrics, is indeed stronger in males than in females and that it is evolutionarily tied to sex biases in parental care and sexual dimorphism. Our findings provide the first comprehensive evidence that Darwin’s concept of conventional sex roles is accurate and refute recent criticism of sexual selection theory.

EVOLUTIONARY LINKS BETWEEN REPRODUCTIVE MORPHOLOGY, ECOLOGY AND MATING BEHAVIOR IN OPISTHOBRANCH GASTROPODS

Abstract Sexual coevolution in morphological and behavioral traits has rarely been studied. Using phylogenetic analyses, we explore relationships between sexual characters based on a new molecular phylogeny of 33 opisthobranch taxa (Aglajidae and Gastropteridae). Our measurements of these simultaneous hermaphrodites include male and female reproductive anatomy, mating behavior, and spatial gregariousness. After phylogenetic correction, we found evidence for correlated evolution between male and female reproductive organs such as the size of the seminal fluid producing prostate gland and that of the sperm digesting bursa copulatrix. Our findings suggest that reproductive trait variation is mediated by sexual coevolution, where putatively manipulative male organs evolved in association with female organs involved in sperm selection. Furthermore, low gregariousness was associated with long, reciprocal copulations. We interpret this result as an adaptation to infrequent mate encounters, where it pays to mate longer with and presumably transfer more sperm to a rare partner. Several complex reproductive traits were repeatedly gained or lost across our phylogeny. This pattern is consistent with a scenario in which sexual selection generates dynamic coevolutionary cycles similar to those expected under sexual antagonism. We finally outline approaches for experimentally assessing the proposed functional links that underlie the evolutionary correlations revealed by our study.

Mate choice and reproductive conflict in simultaneous hermaphrodites

Simultaneous hermaphroditism defines sexual systems in which animals display male and female sex at the same time. Given that each individual now inherently expresses the ‘interests’ of both sexes, this form of gender expression can have profound consequences for the evolution of behavioural reproductive strategies. The outcome of reproductive interactions between two hermaphrodites is likely to vary with (i) intra-individual trade-offs between male and female reproduction, (ii) inter-individual courtship and mate choice between the sexes, (iii) inter-individual competition within the sexes, and (iv) competition with rival individuals in the social group. While earlier work has argued that precopulatory mate choice may only be weakly expressed in simultaneous hermaphrodites, the first section of the chapter documents that, instead, mate choice is prevalent and may include sophisticated mate discrimination based on traits such as body size, mating history, or relatedness. The second section illustrates putative conflicts that individuals may face during copulation, primarily focussing on the decision over mating roles that is central to understand hermaphrodite reproductive behaviour. Available evidence indicates that conditional reciprocity, where individuals accept matings in their disfavoured mating role in order to achieve access to their favoured role, are less widespread than initially though. The final section explores the idea that simultaneous hermaphroditism should enhance selection on postcopulatory mate choice and sperm discrimination mechanisms, including harmful male mating strategies. Support for this prediction remains limited to date, calling for much broader empirical quantifications of the fitness costs and benefits associated with hermaphrodite mating strategies.

Accessory male investment can undermine the evolutionary stability of simultaneous hermaphroditism

Sex allocation (SA) models are traditionally based on the implicit assumption that hermaphroditism must meet criteria that make it stable against transition to dioecy. This, however, puts serious constraints on the adaptive values that SA can attain. A transition to gonochorism may, however, be impossible in many systems and therefore realized SA in hermaphrodites may not be limited by conditions that guarantee stability against dioecy. We here relax these conditions and explore how sexual selection on male accessory investments (e.g. a penis) that offer a paternity benefit affects the evolutionary stable strategy SA in outcrossing, simultaneous hermaphrodites. Across much of the parameter space, our model predicts male allocations well above 50 per cent. These predictions can help to explain apparently ‘maladaptive’ hermaphrodite systems.