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.     

Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction

Although species with both male and female sexual functionsare often dichotomized into simultaneous and sequential hermaphrodites,many simultaneous hermaphrodites also exhibit sequential changesin sex allocation. In a field experiment using one such species,the gobiid fish, Lythrypnus dalli, female-biased individualsreallocated to male function in relation to their relative bodysize: consistent with the sizeadvantage hypothesis, large femaleswere more likely to reallocate and large fish had the highestspawningrates. Individuals, despite internal allocation to bothsexual functions, adopted only one behavioral gender. Behavioralmales had higher reproductive rates than behavioral females,and laboratory experiments showed that females preferred tomate with large males. Behavioral males grew more rapidly anddid notdiffer from behavioral females in survivorship. In addition,individuals who adopted male behavior but did not receive eggsin their nests maintained high levels of female tissue, whereasmales that received eggs did not. Laboratory experiments showedthat, unlike most hermaphroditic animals, L. dalli canchangeallocation either from ‘female’ to ‘male’or from ‘male’ to ‘female’. Thus, L.dalli shares haracteristics of both sequential and simultaneoushermaphrodites. Simultaneous hermaphroditism maybe maintained,in this species, to facilitate rapid sex change from femaleto male and to retain flexibility o that unsuccessful malescan revert to reproduction as females.     

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.     

The rapid dissolution of dioecy by experimental evolution

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Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons?

In the earthworm Lumbricus terrestris L., mating occurs on the soil surface, but partners remain anchored in their burrow andmating is preceded by repeated mutual burrow visits betweenneighbors. This study focuses on body size as one possibletrait that earthworms may assess during these burrow visits.Size-related mate choice is predicted to result in size-assortativemating, which we found in one field sample (n = 90 pairs),but not in a second (n = 102). We discovered that when mates separate, one of them can be pulled out of its burrow. Thiswas more likely for small individuals or those mating acrosswide distances. In a subsequent greenhouse experiment, we allowedfocal individuals to mate with two neighbors of different sizes.Relative size affected neither mating rate nor primary preference,but focals mated sooner with the same-sized neighbor than witha differently sized one. Small focals visited large neighborsmore often than small ones. We conclude that size influencesmate choice as well as the outcome of mating and discuss howthe "tug-of-war" that ends a mating contributes to this result.Precopulatory visits may involve assessment as well as enticementto lure the partner closer to the individual's own burrow,in order to minimize the risk when mating with a partner thatis large or far away.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Alternative reproductive styles in seabreams (Pisces: Sparidae)

Synopsis A review of sexuality in the Sparidae shows that protandrous, protogynous, simultaneous and rudimentary hermaphroditism have all been reported in the family. Careful histological study shows that even in those species reputed to have separate sexes, intersexuality is found in the juvenile condition. We suggest that two reproductive styles, sex change and late gonochorism are found in the family. The bi-potentiality of the sparid gonad is considered to be a pre-adaptation for the development of sequential hermaphroditism in species in which reproductive success is size related. In these species sex change is an alternative reproductive style that enables individuals to maximise their lifetime reproductive success by functioning as one sex when small and the other sex when large.     

Sex Allocation in Lythrypnus (Gobiidae): Variations on a Hermaphroditic Theme

The gonadal sexual patterns of three Atlantic/Caribbean Lythrypnus (L. nesiotes, L. phorellus, L. spilus) are described, based on histological examination, and compared with previously described sexual patterns of L. dalli and L. zebra, from the eastern Pacific. Overall, there was striking similarity in the sexual patterns of all the species; each exhibited simultaneous hermaphroditism with a high degree of variability in allocation to male tissue among individuals. Among the five species whose sexual patterns are described, at least three distinct sexual patterns were identified. Lythrypnus dalli has an allocation pattern distinct from the other species, with populations consisting of primarily pure females, strongly female-biased hermaphrodites and pure males. Lythrypnus nesiotes was also found to be distinct from the other species, consisting primarily of pure females and strongly female-biased hermaphrodites and male-biased individuals (mean allocation to male tissue = 75%). In contrast to L. dalli, L. nesiotes had no pure males. Indeed, no other species examined included pure males. L. phorellus, L. spilus and L. zebra had much more intermediate allocation patterns than either L. dalli or L. nesiotes. Most individuals were female biased (<10% male tissue), and there were significant numbers of individuals with intermediate allocation (10–90% male). L. zebra differed somewhat from L. phorellus and L. spilus in that more strongly male-biased individuals were common in the sample (i.e., ranging in allocation from 90 to 98% male); this difference was not statistically compelling. This marked variation in allocation among closely related species suggests Lythrypnus is a useful model system to explore factors affecting allocation. For example, models developed for simultaneous hermaphrodites and appropriate for Lythrypnus predict that pure sexed individuals will be more common at higher density (e.g., because mating success is more certain). The observed interspecific variation supports this prediction – both L. dalli and L. nesiotes occur at high density and have the most extreme allocation patterns, whereas L. phorellus, L. spilus, and L. zebra occur at lower density and have more intermediate allocation patterns.     

Sex differences in behaviour as an indirect consequence of mating system

A considerable literature has been devoted to documenting differences between the sexes. However, relatively little attention has hitherto been directed towards those differences that arise as an indirect consequence of mating system even though they can have profound implications for the daily lives of the animals involved. In this review we focus on differences in the non-reproductive behaviour of fish and relate these to sexual dimorphism in size and morphology, and to variance in fitness between the sexes. In line with our expectation, differences in distributional ecology, schooling, aggression, predator avoidance and foraging are exaggerated in sexually dimorphic species and polygamous mating systems. Nonetheless, the behaviour of males and females may also differ in sexually monomorphic and monogamous species. We conclude by highlighting promising directions for further research.     

Sex-reversal and androgenic gland in the fish parasite Irona far (cymothoidae: isopoda: crustacea)

The sequence of changes in the primary and secondary sexual characters of the parasitic isopod Irona far during sex-reversal indicate that it is synchronised with the degeneration of the androgenic gland. The gonad is typically hermaphroditic. During the male stage the testicular utricles are large and active but the ovarian region remains undifferentiated. During the intermediate stage production of sperms is stopped and the ovarian region produces ova but without vitellogenesis in them. In the female stage the testicular utricles regress, ovary enlarges and there is increase in egg production and vitellogenesis. The male secondary sexual characters become highly developed during the male stage, regress in the intermediate stage, and finally disappear in the late female stage. Only during the female stage does the female secondary sexual character, viz, the oostegites appear. The androgenic gland shows signs of maximum secretion during the prepuberal and puberal male stages and least activity during the intermediate and early female stages, leading ultimately to total degeneration in the late female stage.