Hybridization between previously isolated ancestors may explain the persistence of exactly two ancient lineages in the genome of the oyster parasite Perkinsus marinus

Authors: Thompson, Peter; HARE, M - Cornell University; Rosenthal, Benjamin

Submitted to: Infection, Genetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/29/2014
Publication Date: 6/30/2014
Publication URL: http://ac.els-cdn.com/S1567134814000859/1-s2.0-S1567134814000859-main.pdf?_tid=b9efa1ac-0dbf-11e4-b70f-00000aab0f6c&acdnat=1405607963_76ebb49eca2ba646273d81075d1f12aa
Citation: Thompson, P.C., Hare, M.P., Rosenthal, B.M. 2014. Hybridization between previously isolated ancestors may explain the persistence of exactly two ancient lineages in the genome of the oyster parasite Perkinsus marinus. Infection, Genetics and Evolution. 24:167-176.

Interpretive Summary: Large biological populations that have not been subdivided should have accumulated variation in different genetic loci. Population samples should identify some loci lacking in variation, others characterized by a few alleles, and still others by many alleles. Departures from these expectations require explanation. Here, we report a striking deviation from these expectations in each of several genes characterized from Perkinsus marinus, an important parasite of oysters and the cause of Dermo disease. In each case, these two alleles differed very substantially (by 3.8%, on average), suggesting that they began diverging millions of years ago. Recombination was concluded to have been responsible distributing these common and alternative alleles into ten distinct multilocus combinations. However, we found no evidence for recombination ever having occurred within any locus. Having considered several alternative demographic and selective hypotheses, we believe these striking data can best be interpreted as evidence that two, long-diverged lineages of P. marinus hybridized, and have subsequently further diversified through at least occasional sexual recombination. Transporting oysters may facilitate contact among evolutionarily independent parasite lineages, a possibility that deserves further attention considering the economic and ecological damage wrought by a disease that is hindering efforts to restore critical estuarine habitats with oysters, a keystone species. These results will be of interest to parasitologists, evolutionary biologists, fisheries managers, and those working to restore Chesapeake Bay and other estuaries.

Technical Abstract: Large biological populations that have not been subdivided should have accumulated variation in different genetic loci. Population samples should identify some loci lacking in variation, others characterized by a few alleles, and still others by many alleles. Departures from these expectations require explanation. Here, we report a striking deviation from these expectations in each of several genes characterized from Perkinsus marinus, an important parasite of oysters and the cause of Dermo disease. In order to examine nucleotide sequence diversity across the genome of P. marinus, establish the extent of allelic dimorphism, and assess potential causes of this pattern, DNA sequences were collected from seven nuclear loci (five of which flank microsatellite repeats and two of which code for superoxide dismutases that may mediate the parasite’s interaction with its host). Only two haplotypes (a common allele ranging in frequency from 72-92% and an alternative allele) were observed more than once in a population sample that spanned most of the continental range of this parasite. In each case, these two alleles differed very substantially (by 3.8%, on average), suggesting that they began diverging millions of years ago. Across these seven loci, only five other haplotypes were ever observed, differing from the common or alternate allele by no more than two nucleotides. Recombination was concluded to have been responsible distributing these common and alternative alleles into ten distinct multilocus combinations. However, we found no evidence for recombination ever having occurred within any locus. Having considered several alternative demographic and selective hypotheses, we believe these striking data can best be interpreted as evidence that two, longdiverged lineages of P. marinus hybridized, and have subsequently further diversified through at least occasional sexual recombination. Transporting oysters may facilitate contact among evolutionarily independent parasite lineages, a possibility that deserves further attention considering the economic and ecological damage wrought by a disease that is hindering efforts to restore critical estuarine habitats with oysters, a keystone species.