Mature habitats associated with genetic divergence despite strong dispersal ability in an arthropod

Abstract

Abstract Background Populations may be bound by contemporary gene flow, selective sweeps, and extinction-recolonization processes. Indeed, existing molecular estimates indicate that species with low levels of gene flow are rare. However, strong priority effects and local selective regimes may hinder gene flow (despite dispersal) sending populations on independent evolutionary trajectories. In this scenario (the monopolization hypothesis), population differentiation will increase with time and genealogical evidence should yield ample private haplotypes. Cyclical parthenogens (e.g. rotifers and cladocerans such as Daphnia) have an increased capacity for rapid local adaptation and priority effects because sexual reproduction is followed by multiple generations of clonal selection and massive egg bank formation. We aimed to better understand the history of population differentiation and ongoing gene flow in Daphnia rosea s.l., by comparing population and regional divergences in mature unglaciated areas and younger previously glaciated areas. We also examined the timing and paths of colonization of previously-glaciated areas to assess the dispersal limitations of D. rosea s.l. We used DNA sequence variation (84 populations and >400 individuals) at the mitochondrial ND2 and nuclear HSP90 loci from Holarctic populations for our genetic analyses. Results The genetic evidence indicated pronounced historical structure. Holarctic mtDNA phylogenies of D. rosea s.l. revealed three geographically restricted and divergent clades: European, Siberian and Japanese/American. The Japanese/American clade showed marked population genetic structure (FST > 0.8) that was weakly associated with geographic distance, and a high proportion of private haplotypes. Populations from older unglaciated habitats (i.e., Japan) showed higher DNA sequence divergences than populations from presumed younger habitats (i.e. non-Beringian North America) with nDNA and with mtDNA. Mismatch analyses of mtDNA and nDNA were consistent with a single rapid post-glacial expansion of D. rosea that covered most of the New World. Conclusion Our evidence agrees with negligible gene flow after founding, and the accumulation of genetic divergence with habitat age. Existing direct evidence and our mismatch analyses indicate that the pronounced population differentiation is unlikely to be due to dispersal limitation. Instead, priority effects and local selection regimes may play a role in limiting gene flow. The results challenge the notion that lacustrine populations of cladocerans are generally unified by contemporary gene flow.