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

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.