Demographic history shapes genomic variation in an intracellular parasite with a wide geographical distribution

Abstract

Analysing variation in a species’ genomic diversity can provide insights into its historical demography, biogeography and population structure, and thus its ecology and evolution. Although such studies are rarely undertaken for parasites, they can be highly revealing because of the parasite's co‐evolutionary relationships with hosts. Modes of reproduction and transmission are thought to be strong determinants of genomic diversity for parasites and vary widely among microsporidia (fungal‐related intracellular parasites), which are known to have high intraspecific genetic diversity and interspecific variation in genome architecture. Here we explore genomic variation in the microsporidium Hamiltosporidium, a parasite of the freshwater crustacean Daphnia magna, looking especially at which factors contribute to nucleotide variation. Genomic samples from 18 Eurasian populations and a new, long‐read‐based reference genome were used to determine the roles that reproduction mode, transmission mode and geography play in determining population structure and demographic history. We demonstrate two main Hamiltosporidium tvaerminnensis lineages and a pattern of isolation‐by‐distance, but note an absence of congruence between these two parasite lineages and the two Eurasian host lineages. We suggest a comparatively recent parasite spread through Northern Eurasian host populations after a change from vertical to mixed‐mode transmission and the loss of sexual reproduction. While gaining knowledge about the ecology and evolution of this focal parasite, we also identify common features that shape variation in genomic diversity for many parasites, such as distinct modes of reproduction and the intertwining of host–parasite demographies.

Genetic Drift Shapes the Evolution of a Highly Dynamic Metapopulation

“…Between 72% and 99% of our pool-seq reads were mapped to the D. magna reference genome (supplementary table S1, Supplementary Material online). Samples with a low mapping percentage were infected with a locally common microsporidian parasite (Hamiltosporidium tvaerminnensis; supplementary table S1, Supplementary Material online) that can dominate the sequencing reads when whole genomes of host and parasites are cosequenced (Angst et al 2022). With only a few exceptions, the average read coverage for most D. magna samples was beyond 20× (supplementary table S1, Supplementary Material online).…”

Genetic drift shapes the evolution of a highly dynamic metapopulation

“…Between 72 and 99 % of our pool-seq reads were mapped to the D. magna reference genome (Table S1). Samples with a low mapping percentage were infected with a locally common microsporidian parasite ( Hamiltosporidium tvaerminnensis ; Table S1) that can dominate the sequencing reads when whole genomes of host and parasites are co-sequenced (Angst et al, 2022). With only a few exceptions, the average read coverage for most D. magna samples was beyond 20× (Table S1).…”

Population Genetics of Parasites and Their Arthropod Hosts

“…Parasites with tight host-parasite interactions, but incongruent population structuring may provide important insights into the host's history. Such is the case with the microsporidian Hamiltosporidium tvaerminnensis Haag, parasitising the cladoceran Daphnia magna, where the observed incongruence may stem from a switch to different mode of reproduction and transmission, though it may also indicate the existence of another glacial refugium for D. magna [43]. The existence of cryptic lineages of the cycliophoran Symbion Funch & Kristensen specific to certain lobster species may also indicate the host species' history during Pleistocene glaciations [44,45].…”