Microsatellite and single‐nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite

Abstract

Assessing the mode of reproduction of microparasites remains a difficult task because direct evidence for sexual processes is often absent and the biological covariates of sex and asex are poorly known. Species with geographically divergent modes of reproduction offer the possibility to explore some of these covariates, for example, the influence of life-history traits, mode of transmission and life-cycle complexity. Here, we present a phylogeographical study of a microsporidian parasite, which allows us to relate population genetic structure and mode of reproduction to its geographically diverged life histories. We show that in microsporidians from the genus Hamiltosporidium, that use the cladoceran Daphnia as host, an epidemic population structure has evolved, most probably since the last Ice Age. We partially sequenced three housekeeping genes (alpha tubulin, beta tubulin and hsp70) and genotyped seven microsatellite loci in 51 Hamiltosporidium isolates sampled within Europe and the Middle East. We found two phylogenetically related asexual parasite lines, one each from Fennoscandia and Israel, which share the unique ability of being transmitted both vertically and horizontally from Daphnia to Daphnia. The sexual forms cannot transmit horizontally among Daphnia, but presumably have a complex life cycle with a second host species. In spite of the similarities between the two asexual lineages, a clustering analysis based on microsatellite polymorphisms shows that asexual Fennoscandian parasites do not share ancestry with any other Hamiltosporidium that we have sampled. Moreover, allele sequence divergence at the hsp70 locus is twice as large in Fennoscandian than in Israeli parasites. Our results indicate that asexual reproduction evolved twice independently, first in Fennoscandian and more recently in the Israeli parasites. We conclude that the independent origin of asexuality in these two populations is associated with the altered parasite mode of transmission and the underlying dynamics of host populations.

Clonal Evolution of Enterocytozoon bieneusi Populations in Swine and Genetic Differentiation in Subpopulations between Isolates from Swine and Humans

“…Sexual and asexual reproduction alternates in many protozoan species under environmental pressure [47]. It is generally accepted that microsporidia undergo sexual reproduction, whereas some species or genotypes possibly have switched to obligate asexuality [48].…”

“…This is supported by the existence of clonal population structure in SP1 and SP5 and epidemic population structure or host-adapted traits in SP3 to SP4. Although a sexual phase might be rare or virtually absent in some microsporidian species, there are footprints of recombination in their genomes [47,48]. This could be responsible for the small number of recombination inferred in subpopulations SP1 through SP5.…”

Genetic, ecological and geographic covariables explaining host range and specificity of a microsporidian parasite

“…), which has been reported only in Daphnia magna rock pool populations along the eastern Swedish and southern Finnish coast of the Baltic Sea (Ebert ; Haag, Traunecker & Ebert ; Haag et al . ), although its host species is commonly found throughout Eurasia and Africa. A dispersal barrier limiting this parasite to a small geographic region seems unlikely, since the parasite can survive and co‐migrate in the resting eggs of its host (Vizoso, Lass & Ebert ), and D. magna population genetics support high migration rates among European populations (De Gelas & De Meester ).…”

Microsporidia: Eukaryotic Intracellular Parasites Shaped by Gene Loss and Horizontal Gene Transfers

“…More recently, explorations of intragenomic allelic variation have revealed diploidy in many species, including E. cuniculi (78), Nematocida parisii, Nematocida sp1 (18), Hamiltosporidium tvaerminnensis, and H. magnivora (28,29), and polyploidy in Nosema cerena (64). These levels of ploidy suggest that many microsporidia undergo a haploid-diploid cell cycle leading to novel genetic diversity within populations following outcrossing and karyogamy (20,31,32).…”

“…This is unfortunate, because intraspecific genetic diversity (i.e., accumulation of nucleotide www.annualreviews.org • Microsporidian Genome Biology substitutions, copy number polymorphism, aneuploidy, deletions, and insertions) plays a major role in the adaptability of parasites to changes in their surrounding environments and within their hosts. Although population-level analyses of some microsporidian species have recently emerged (28,29,74,78), more efforts in this area are required to fully comprehend the biology of these intracellular parasites and to better prepare countermeasures against potential future outbreaks of these organisms.…”