Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes

Abstract

Background: Physa acuta is a globally invasive freshwater snail native to North America. Prior studies have led to conflicting views of how P. acuta populations are connected and genetic diversity is partitioned globally. This study aims to characterize phylogeographic and population genetic structure within the native range of P. acuta, elucidate its invasion history and assess global patterns of genetic diversity. Further, using meta-analytic methods, we test the 'Enemy-Release hypothesis' within the P. acuta - digenetic trematode system. The 'Enemy-Release hypothesis' refers to the loss of native parasites following establishment of their host within an invasive range. Population genetic data is combined with surveys of trematode infections to map range-wide trematode species richness associated with P. acuta, and to identify relevant host-population parameters important in modeling host-parasite invasion. Results: Phylogenetic analyses using mtDNA uncovered two major clades (A & B). Clade A occurs globally while clade B was only recovered from the Western USA. All invasive populations sampled grouped within Clade A, where multiple independent source populations were identified from across North America. Significant population genetic structure was found within the native range of P. acuta, with some evidence for contemporary geographic barriers between western and eastern populations. Mito-nuclear discordance was found suggesting historical isolation with secondary contact between the two mitochondrial clades. Trematode species richness was found to differ significantly between native and invasive populations, in concordance with the 'Enemy-Release hypothesis'. Further, our data suggests a positive relationship between nucleotide diversity of invasive populations and trematode prevalence and richness. Conclusions: This study includes a wider geographic sampling of P. acuta within its native range that provides insight into phylogeographic and population genetic structure, range-wide genetic diversity and estimation of the invasion history. Meta-analysis of P. acuta - trematode surveys globally is consistent with the 'Enemy-Release hypothesis'. Additionally, results from this study suggest that host demographic parameters, namely genetic diversity as a proxy for population size, may play an essential role in how parasite communities assemble within invasive host populations. This knowledge can be used to begin to construct a framework to model host-parasite invasion dynamics over time.