Lineage divergence, local adaptation across a biogeographic break, and artificial transport, shape the genetic structure in the ascidian Pyura chilensis

Nicolás I Segovia,Pilar A Haye,Cristian Gallardo-Escárate,Elie Poulin

doi:10.1038/srep44559

Abstract

Marine benthic organisms inhabit a heterogeneous environment in which connectivity between populations occurs mainly through dispersive larval stages, while local selective pressures acting on early life history stages lead to non-random mortality, shaping adaptive genetic structure. In order to test the influence of local adaptation and neutral processes in a marine benthic species with low dispersal, in this study we used Genotyping by Sequencing technology to compare the neutral and putatively selected signals (neutral and outlier loci, respectively) in SNPs scattered throughout the genome in six local populations of the commercially exploited ascidian Pyura chilensis along the southeast Pacific coast (24°–42°S). This species is sessile as an adult, has a short-lived larval stage, and may also be dispersed by artificial transport as biofouling. We found that the main signal in neutral loci was a highly divergent lineage present at 39°S, and a subjacent signal that indicated a separation at 30°S (north/south), widely reported in the area. North/south separation was the main signal in outlier loci, and the linage divergence at 39°S was subjacent. We conclude that the geographic structure of the genetic diversity of outlier and neutral loci was established by different strengths of environmental, historical and anthropogenic factors.

Highlights

One experimental approach to analyze neutral and putatively adaptive signals is the use of genome scans to detect thousands of Single Nucleotide Polymorphism (SNP) loci scattered throughout the genome, some of which can be identified as having signals of natural selection by analyzing several individuals from different environments[13]
In contrast to what has been reported for other sympatric benthic species of the Humboldt Current System (HCS) with low larval dispersal capacity[26], P. chilensis did not show a genetic discontinuity at 30°S when analyzed with sequences of the mitochondrial gene Cytochrome Oxidase I (COI) and the nuclear gene Elongation Factor 1 alpha[30]
We evaluate the divergence of the Los Molinos (LM) population of P. chilensis using neutral and putatively adaptive SNP loci, and explore if natural selection follows the same signal as neutral sequence divergence, i.e. if LM is highly differentiated with putatively adaptive loci

Summary

Introduction

One experimental approach to analyze neutral and putatively adaptive signals is the use of genome scans to detect thousands of Single Nucleotide Polymorphism (SNP) loci scattered throughout the genome, some of which can be identified as having signals of natural selection by analyzing several individuals from different environments[13]. This has not been assessed for P. chilensis, the species has often been seen on the hulls of boats of artisanal fisheries, on buoys, ropes and on any other marine facility that provides substratum as an important part of the fouling community[34,35] This has been hypothesized as one of the mechanisms behind the low degree of genetic differentiation of the COI gene along a broad geographic area and across the 30°S biogeographic break[30]; anthropogenic transport has often been suggested as a main dispersal and invasion mechanism for other ascidians[30,31,32,33]. Lack of spatial genetic differentiation at neutral or nearly neutral loci does not imply that outlier loci will provide the same signal[36]

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