Nico K. Michiels

7 – Mating Conflicts and Sperm Competition in Simultaneous Hermaphrodites

This chapter speculates on the consequences of sexual selection and sperm competition in a hermaphroditic mating system. Quantitative data related here, such as mating frequency, sperm transfer, sperm usage and fertilization success, are very rare for hermaphrodites. As a result, it is now generally accepted that sexual selection applies to all types of gender expression. However, hermaphrodites have the unique property that they can optimize their allocation to the male and female function. The chapter explains how conflicts between mating partners arise in hermaphrodites, and why they are particularly strong during copulation because of different mating interests. Hermaphroditic animals are still largely absent from sexual selection literature. It also focuses on why animal taxa deserve a more central place in evolutionary biological literature. Thus, the consequences of sexual selection and sperm competition in a hermaphroditic mating system are expected to be common and that the adaptations resulting from it are sometimes drastic and unique to hermaphrodites. Although constrained in their evolutionary response to sexual selection, it is clear that there is a scope for evolutionary arms races in hermaphrodites that may result in adaptations that are at least as diverse as those seen among gonochorists.

Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite

The coevolution between hosts and parasites is predicted to have complex evolutionary consequences for both antagonists, often within short time periods. To date, conclusive experimental support for the predictions is available mainly for microbial host systems, but for only a few multicellular host taxa. We here introduce a model system of experimental coevolution that consists of the multicellular nematode host Caenorhabditis elegans and the microbial parasite Bacillus thuringiensis. We demonstrate that 48 host generations of experimental coevolution under controlled laboratory conditions led to multiple changes in both parasite and host. These changes included increases in the traits of direct relevance to the interaction such as parasite virulence (i.e., host killing rate) and host resistance (i.e., the ability to survive pathogens). Importantly, our results provide evidence of reciprocal effects for several other central predictions of the coevolutionary dynamics, including (i) possible adaptation costs (i.e., reductions in traits related to the reproductive rate, measured in the absence of the antagonist), (ii) rapid genetic changes, and (iii) an overall increase in genetic diversity across time. Possible underlying mechanisms for the genetic effects were found to include increased rates of genetic exchange in the parasite and elevated mutation rates in the host. Taken together, our data provide comprehensive experimental evidence of the consequences of host–parasite coevolution, and thus emphasize the pace and complexity of reciprocal adaptations associated with these antagonistic interactions.

Regulation of red fluorescent light emission in a cryptic marine fish

IntroductionAnimal colouration is a trade-off between being seen by intended, intra- or inter-specific receivers while not being seen by the unintended. Many fishes solve this problem by adaptive colouration. Here, we investigate whether this also holds for fluorescent pigments. In those aquatic environments in which the ambient light is dominated by bluish light, red fluorescence can generate high-contrast signals. The marine, cryptic fish Tripterygion delaisi inhabits such environments and has a bright red-fluorescent iris that can be rapidly up- and down-regulated. Here, we described the physiological and cellular mechanism of this phenomenon using a neurostimulation treatment with KCl and histology.ResultsKCl-treatment revealed that eye fluorescence regulation is achieved through dispersal and aggregation of black-pigmented melanosomes within melanophores. Histology showed that globular, fluorescent iridophores on the anterior side of the iris are grouped and each group is encased by finger-like extensions of a single posterior melanophore. Together they form a so-called chromatophore unit. By dispersal and aggregation of melanosomes into and out of the peripheral membranous extensions of the melanophore, the fluorescent iridophores are covered or revealed on the anterior (outside) of the iris.ConclusionT. delaisi possesses a well-developed mechanism to control the fluorescent emission from its eyes, which may be advantageous given its cryptic lifestyle. This is the first time chromatophore units are found to control fluorescent emission in marine teleost fishes. We expect other fluorescent fish species to use similar mechanisms in the iris or elsewhere in the body. In contrast to a previously described mechanism based on dendritic fluorescent chromatophores, chromatophore units control fluorescent emission through the cooperation between two chromatophore types: an emitting and an occluding type. The discovery of a second mechanism for fluorescence modulation strengthens our view that fluorescence is a relevant and adaptive component of fish colouration.

Sperm Digestion and Reciprocal Sperm Transfer Can Drive Hermaphrodite Sex Allocation to Equality

The intensity of sperm competition determines how much reproductive effort should be invested in sperm. One important factor affecting sperm competition in internally fertilizing organisms is the mating frequency of females, since it determines the extent of competition between ejaculates. In simultaneous hermaphrodites, energy spent on sperm has to be traded off against energy expended on ova production. By extending an existing model, we consider how the number of matings affects sperm competition and, thus, sex allocation in internally fertilizing simultaneous hermaphrodites. We then go on to explore the consequences of two common characteristics of hermaphroditic mating systems, namely, sperm digestion and reciprocal insemination. Since sperm digestion reduces the competitive ability of a given ejaculate, it selects for increased sperm investment. As a result, the amount of sperm digested and male allocation can enter a coevolutionary cycle in which both will increase up to the point of equal investment in male and female gametes and in high rates of digestion. Because of this high degree of sperm digestion, fitness through the male function becomes more dependent on the amount of resources invested in sperm than on the number of matings. As a result, sperm digestion reduces Batemans principle. Hence, hermaphrodites with sperm digestion should be less likely to display traits that increase the number of matings. Once ejaculates are large and costly, animals insisting on reciprocal sperm transfer will be favored since they receive some compensation for their investment. Under reciprocity, an even higher investment in sperm is favored. This is the result of the compensation received in the form of the partners ejaculate and a nuptial gift effect by increasing a partners production of eggs.

Sex and violence in hermaphrodites

Differences in objectives between males and females are a driving force in the evolution of copulatory mechanisms. Hermaphrodites can also have sexual conflicts, but caused by opposing sexual interests within rather than between individuals. One consequence seems to be that physically damaging sex, as occurs with the marine flatworm Pseudoceros bifurcus, might be favoured more in hermaphrodites than in species with separate sexes.

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.

Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp.

Sex allocation theory for simultaneous hermaphrodites assumes a direct trade‐off between the allocation of resources to the male and female reproductive functions. Empirical support for this basic assumption is scarce, possibly because studies rarely control for variation in individual reproductive resource budgets. Such variation, which can have environmental or genetic sources, can generate a positive relationship between male and female investment and can thus obscure the trade‐off. In this study on the hermaphroditic flatworm Macrostomum sp. we tried to control for budget effects by restricting food availability in a standardized way and by using an inbred line. We then manipulated mating group size in a two‐way design (two group sizes × two enclosure sizes) in order to induce phenotypic variation in male allocation, and expected to find an opposing correlated response in female allocation. The results suggest that we only managed to control the budget effects under some conditions. Under these the sex allocation trade‐off emerged. Under the other conditions we found a strongly positive correlation between male and female allocation. We discuss possible causes for the observed differences.

Flatworms flatten to size up each other

When copulations are costly, fertilization is reciprocal and fecundity is positively related to size, hermaphrodites are expected to favour large partners, leading to size–assortative mating. Size–related mate choice has, however, never been observed in hermaphrodites. In the flatworm Dugesia gonocephala copulations cost time and are reciprocal, and size is a positive predictor of female fecundity. Every copulation is preceded by a phase in which one partner glides on top of the other and both spread out and flatten, suggesting that partners assess each others size. A total of 124 copulating pairs collected on four different dates, proved that mating is size–assorted in the field. In experiments with groups, more copulations took place between equally sized individuals than were expected when matings were random. In experiments with pairs, partners of different size exhibited twice as many mating attempts for the first copulation than did partners of the same size. We conclude that D. gonocephala employs a unique kind of pre–copulatory ‘flattening’ behaviour as a mechanism to signal as well as to assess relative size. This does not only confirm that hermaphrodites can mate assortatively when certain assumptions are met, it also proves that even lower invertebrates can show active mate choice.

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.

Low potential for sexual selection in simultaneously hermaphroditic animals

Hermaphroditic animals are poorly represented in the sexual selection literature. This deficiency may reflect our inability to come to grips with hermaphroditism or, alternatively, it could be due to an inherent difference between hermaphrodites and gonochorists. Here we provide a number of reasons why sexual selection on traits related to mate acquisition can be expected to be intrinsically weaker in hermaphrodites. We show that the ‘male’ fitness component, which can be increased by sexual selection in hermaphrodites, is only half that of pure males in a gonochorist population. This component can be reduced even further when hermaphrodites self–fertilize. As a result, the potential for sexual selection (ψ) on male characters in hermaphrodites is at most half that of gonochorists. Given a specific mate handling cost, sperm production cost and rate of encountering receptive mates, we calculate the optimal allocation to mate acquisition and sperm. Since both partners of a hermaphroditic pair invest in mate acquisition, hermaphrodites should optimally invest less in mate acquisition. This can further reduce ψ by up to one–half. A higher readiness to mate and high investment in sperm can lead to a further systematic reduction in Ps in hermaphrodites.