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

Parasitology. 2018 Mar;145(3):408-415. doi: 10.1017/S0031182017001597. Epub 2017 Sep 25.

Abstract

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.

Keywords: Paramyxid; co-infection; feminization; intersex; microsporidian; sex-ratio.

MeSH terms

  • Amphipoda / parasitology
  • Animals
  • Coinfection / epidemiology
  • Coinfection / parasitology*
  • Disorders of Sex Development / parasitology*
  • Female
  • Feminization / parasitology*
  • France / epidemiology
  • Host-Parasite Interactions
  • Male
  • Microsporidia / physiology*
  • Prevalence
  • Sex Ratio