Microsporidian parasites feminise hosts without paramyxean co-infection: support for convergent evolution of parasitic feminisation

Abstract

Feminisation of amphipod crustaceans is associated with the presence of at least three microsporidian parasites and one paramyxean parasite, suggesting that the ability to feminise has evolved multiple times in parasites of amphipods. Co-infection by a paramyxean with one of the putative microsporidian feminisers, Dictyocoela duebenum, has inspired the alternative hypothesis that all feminisation of amphipods is caused by paramyxea and that all microsporidian associations with feminisation are due to co-infection with paramyxea (Short et al., 2012). In a population of the amphipod Gammarus duebeni, breeding experiments demonstrate that the microsporidia D. duebenum and Nosema granulosis are associated with feminisation in the absence of paramyxea. Co-infection of the two microsporidia is no more frequent than expected at random and each parasite is associated with feminisation in the absence of the other. These findings support the original hypothesis that the ability to feminise amphipods has evolved in microsporidia on multiple occasions. Additionally, the occurrence of a non-feminising strain of D. duebenum in Gammarus pulex suggests that different strains vary in their feminising ability, even within microsporidian species. The presence or absence of feminising ability in a particular microsporidian strain should not therefore be generalised to the species as a whole.

Correlations between estrogen and testosterone concentrations, pairing status and acanthocephalan infection in an amphipod

“…Our results should be interpreted with some caution, as we only recorded amphipods with visible cystacanths. Other parasites, such as microsporidians and paramyxeans, feminize male amphipods (Terry et al ., ; Ironside & Alexander, ) and could also impact endocrine pathways. Acanthocephalan parasites impact male–male competition for mates and propensity for pairing in G. pulex (Bollache et al ., ), changes that could hypothetically correlate with reduced testosterone or increased estradiol concentrations if the hormones function analogously in crustaceans and vertebrates.…”

A Microsporidian blocksPlasmodium falciparumtransmission inAnopheles arabiensismosquitoes

“…Species with solely horizontal transmission usually show greater virulence and lower host specificity, but where a combination of horizontal and vertical transovarial transmission occurs, lower virulence is advantageous, and is normally associated with a higher degree of host specificity 11–12 . Sex ratio distortion toward females has been reported (a manipulation characteristic of transovarially transmitted symbionts), for example Dictyocoela microsporidia in Amphipod crustaceans 13 . Various microsporidia species have been reported in mosquitoes 14–25 , with simple or complex lifecycles 14 but all of which are pathogens where virulence is primarily associated with larval mortality or reduced adult fecundity and lifespan 14–20 .…”

Population screening and transmission experiments indicate paramyxid-microsporidian co-infection in Echinogammarus marinus represents a non-hyperparasitic relationship between specific parasite strains

“…Some are horizontally transmitted pathogens that cause substantial mortalities in economically important species 2 , 3 while others are vertically transmitted and have less destructive impacts on their hosts. For example, some microsporidians subvert the amphipod sex determination mechanism and convert males into females 4 , 5 . This feminising capacity appears to have evolved independently in several microsporidian lineages, including strains of Nosema granulosis and Dictyocoela duebenum 4 – 6 .…”

“…For example, some microsporidians subvert the amphipod sex determination mechanism and convert males into females 4 , 5 . This feminising capacity appears to have evolved independently in several microsporidian lineages, including strains of Nosema granulosis and Dictyocoela duebenum 4 – 6 . This strategy is thought to have evolved to allow parasites to maximise their transmission via the host’s progeny by converting males into reproductive females 7 .…”

“…When parasites possess similar life cycles and infect the same host it can favour the evolution of a ‘hitchhiking’ strategy 14 . Given the associations between paramyxids, microsporidians and amphipod feminisation 4 , 8 , it is possible that one of these parasites is a more efficient feminiser in any given host species or environment. This scenario would allow the hitchhiker to benefit from the feminising capacity of its co-infecting parasite.…”