Genome-wide Assessment Elucidates Connectivity and the Evolutionary History of the Highly Dispersive Marine Invertebrate Littoraria Flava (Littorinidae:Gastropoda)

Abstract

Background: An important goal of population genetics studies in marine ecosystems is understanding how connectivity patterns, both spatial and temporal, are influenced by historical and evolutionary factors. When it comes to dispersion and connectivity in marine ecosystems, the role of historical and evolutionary factors over population dynamics andstructure still remains enigmatic. We evaluated the demographic history and population structure of Littoraria flava, a highly dispersive and widely distributed marine gastropod on the Brazilian intertidal zone, to predict the effects of such factors on intrapopulation divergence. To test the hypotheses that (1) the species has historically high levels of geneflow on a macrogeographic spatial scale and (2) the species distribution in rocky shores consists of subpopulations due to high degrees of environmental heterogeneity, we collected specimens along the Brazilian coastline and combined different sets of genetic markers (mitochondrial DNA, nuclear internal transcribed spacer 2, and single nucleotide polymorphisms) with niche-based modeling to predict species paleodistribution.Results: Low genetic structure was observed along the coastline, and all clustering and migration analyses supported the high gene flow over long distances hypothesis (> 3,000 km). Three genetic clusters were identified by the assignment test, each mostly composed of individuals from the three sampled regions. No fine-scale variation was observed for any location. The neutrality tests and the haplotype networks suggest that L. flava had experienced population bottleneck followed by population expansion. Both paleodistribution and coalescent simulations highlight that expansion events occurred in the Southeastern coastline during the Pleistocene interglacial cycles (21 kya).Conclusions: This is the first study on the South American coast that highlights the demographic history on a marine gastropod based on genomic markers associated with niche modelling. We found that climatic changes since the interglacial periods are potentially relevant drivers for the species distribution in the past. Our findings could enhance the understanding of the population dynamics under an evolutionary view for widely distributed non-model marine organisms.