Parasitism-Induced Intersexuality in a Sexually Dimorphic Varunid Crab, Ptychognathus ishii (Decapoda: Varunidae).

Although many animals that perform sexual reproduction exhibit sexual dimorphism, individuals with intersex traits between the traits of males and females appear in some species, depending on environmental factors. Ptychognathus ishii, a varunid crab, exhibits distinctive sexual dimorphism in the morphology of its abdomen, chelipeds and setal tufts on the chelipeds. In this study, however, we report for the first time that intersex individuals with intermediate characters between those of males and females were occasionally found in wild populations. Morphological features of intersex individuals are described. Their taxonomic positions are identified based on DNA sequences of part of the mitochondrial cytochrome c oxidase I (COI) gene. It was shown that the intersexuality was induced by entoniscid parasites, because all intersex individuals were parasitized by entoniscid isopods, identified as Entionella sp. The apparent correlation between parasitism and morphological anomalies suggests that the parasitic isopods affect physiological conditions, leading to the feminization of male hosts.

Multiple origins of parasitic feminization: thelygeny and intersexuality in beach-hoppers are caused by paramyxid parasites, not microsporidia.

Within populations of the amphipod crustaceans Orchestia gammarellus and Orchestia aestuarensis, a proportion of females produce thelygenic (female-only) broods, which often contain intersexual individuals. This phenomenon is associated with the presence of two putative feminizing parasites, the paramyxid Paramarteilia orchestiae and the microsporidian Dictyocoela cavimanum, which frequently co-infect the same host. In order to determine which of the parasites causes feminization, Orchestia were resampled from the type locality of P. orchestiae in France and from another population in the UK. Breeding experiments indicated that female O. gammarellus infected with P. orchestiae produced a significantly higher proportion of female and intersex offspring than uninfected females, even in the absence of D. cavimanum. There was no difference in mortality between infected and uninfected broods, indicating that the paramyxid alters the sex ratio through feminization rather than male-killing. Although D. cavimanum also displays a female-biased prevalence in Orchestia populations, this is due to co-infection with P. orchestiae, indicating that the paramyxid, rather than the microsporidian, is the cause of feminization in these Orchestia populations.

A widespread and distinctive form of amphipod intersexuality not induced by known feminising parasites.

Intersexuality occurs in a diverse range of animals, and its study offers insights into basic reproductive biology. Investigations in amphipods suggest intersexuality results from incomplete feminisation caused by sex-distorting parasites. It has also been noted that 2 intersex phenotypes occur in males of the amphipod Echinogammarus marinus, an external phenotype, in which males possess rudimentary brood plates, and an internal phenotype, in which only an ovotestis is present. This study examines the relationship between these phenotypes and finds their prevalences are independent. In addition, a cross-species microarray reveals the testicular transcriptomes of the intersex phenotypes are distinct from that of normal males and, most crucially, each other. Furthermore, the internal intersex phenotype, unlike the external phenotype, shows no correlation with infection by known feminising parasites. These findings suggest the male intersex phenotypes should not be considered stages on a single spectrum of intersexuality. Rather, they support the hypothesis that internal and external intersexuality are divergent phenotypes with separate causal mechanisms and point to the existence of a distinct and geographically widespread form of amphipod intersexuality caused by an unknown factor.

Parasite infection, host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite.

Parasites have been proposed to be fundamental in the evolution of mate choice because differential mating on the basis of heritable disease resistance is expected to lead to progeny with a better genome-environment match than random mating. However, direct empirical data in support of this hypothesis are often lacking, and the relative influences of current and potential infection status (i.e. resistance genotype), and of mate choice versus mate conflict, remain largely unknown. We demonstrate experimentally, using simultaneous hermaphroditic snails (Biomphalaria glabrata) artificially selected for resistance or susceptibility to Schistosoma mansoni infection, that mate choice is influenced by a combination of current and potential parasitic infection status. As predicted by game-theory models, we also found a picture of conflict and cooperation: resistant and susceptible genotypes copulated in either gender and reciprocated (i.e. switched gender) equally when faced with an uninfected partner, but, by contrast, resistant snails actively refused to copulate as females with an infected partner. Such recognition and discrimination has implications for the maintenance of sex and the evolution of recognition systems.