Co-phylogeographic structure in a disease-causing parasite and its oyster host

Abstract

With the increasing affordability of next-generation sequencing technologies, genotype-by-sequencing has become a cost-effective tool for ecologists and conservation biologists to describe a species' evolutionary history. For host–parasite interactions, genotype-by-sequencing can allow the simultaneous examination of host and parasite genomes and can yield insight into co-evolutionary processes. The eastern oyster, Crassostrea virginica, is among the most important aquacultured species in the United States. Natural and farmed oyster populations can be heavily impacted by ‘dermo’ disease caused by an alveolate protist, Perkinsus marinus. Here, we used restricted site-associated DNA sequencing (RADseq) to simultaneously examine spatial population genetic structure of host and parasite. We analysed 393 single-nucleotide polymorphisms (SNPs) for P. marinus and 52,100 SNPs for C. virginica from 36 individual oysters from the Gulf of Mexico (GOM) and mid-Atlantic coastline. All analyses revealed statistically significant genetic differentiation between the GOM and mid-Atlantic coast populations for both C. virginica and P. marinus, and genetic divergence between Chesapeake Bay and the outer coast of Virginia for C. virginica, but not for P. marinus. A co-phylogenetic analysis confirmed significant coupled evolutionary change between host and parasite across large spatial scales. The strong genetic divergence between marine basins raises the possibility that oysters from either basin would not be well adapted to parasite genotypes and phenotypes from the other, which would argue for caution with regard to both oyster and parasite transfers between the Atlantic and GOM regions. More broadly, our results demonstrate the potential of RADseq to describe spatial patterns of genetic divergence consistent with coupled evolution.

Keywords: Crassostrea virginica; Perkinsus marinus; co-phylogeny; genetic divergence; genotype-by-sequencing.

Graphical abstract

Figure 1.

Map of geographic location of each site collection for the region of Virginia [circle, Chesapeake Bay; squares, Eastern Shore; red, Fleet Point (n = 2); yellow, VIMS Beach (n = 11); orange, Wreck Shoal (n = 1); black, Broad Creek (n = 1); purple, Wachapreague (n = 1); blue, Oyster (n = 6)] and 2 regions in the Gulf of Mexico [red = Louisiana (n = 5) and black = Alabama (n = 3)].

Figure 2.

Principal components analyses of (A) Perkinsus marinus (393 loci, n = 36) from PCangsd and (B) Crassostrea virginica (52100 SNPs, n = 35) from prcomp.

Figure 3.

Admixture analysis of (A) Perkinsus marinus (393 loci, n = 36) using genotype likelihoods in NGSadmix and (B) Crassostrea virginica (52100 SNPs, n = 35) using genotypes in SNMF.

Figure 4.

A maximum-likelihood co-phylogeny of the parasite Perkinsus marinus (392 bp) and host Crassostrea virginica (52052 bp). All nodes have 100% consensus support for C. virginica while all nodes have <50% support for P. marinus (1000 bootstrap replicates for both). Black and red dashed lines indicate GOM and VA genotypes within Crassostrea, respectively, and linked to Perkinsus genotypes.