Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands

Karin Gérard,Alexandra Anh-Thu Weber,Nicolas Bierne,Anne Chenuil,Christelle Fraïsse,Anne Haguenauer

doi:10.24072/pcjournal.18

Abstract

Reticulated evolution -i.e. secondary introgression / admixture between sister taxa-is increasingly recognized as playing a key role in structuring infra-specific genetic variation and revealing cryptic genetic connectivity patterns. When admixture zones coincide with ecological transitions, the connectivity patterns often follow environmental variations better than distance and introgression clines may easily be confounded with local adaptation signatures. The Kerguelen mussels is an ideal system to investigate the potential role of admixture in enhancing micro-geographic structure, as they inhabit a small isolated island in the Southern Ocean characterized by a highly heterogeneous environment. Furthermore, genomic reticulation between Northern species (M. edulis, M. galloprovincialis and M. trossulus) and Southern species (M. platensis: South America and the Kerguelen Islands; and M. planulatus: Australasia) has been suspected. Here, we extended a previous analysis by using targeted-sequencing data (51,878 SNPs) across the three Northern species and the Kerguelen population. Spatial structure in the Kerguelen was then analyzed with a panel of 33 SNPs, including SNPs that were more differentiated than the genomic average between Northern species (i.e., ancestry-informative SNPs). We first showed that the Kerguelen lineage splitted very shortly after M. edulis and M. galloprovincialis initiated speciation, and it subsequently experienced admixture with the three Northern taxa. We then demonstrated that the Kerguelen mussels were significantly differentiated over small spatial distance, and that this local genetic structure was associated with environmental variations and mostly revealed by ancestry-informative markers. Simulations of admixture in the island highlight that genetic-environment associations can be better explained by introgression clines between heterogeneously differentiated genomes than by adaptation.

Highlights

Marine species with planktonic larvae are high-dispersal organisms, with large effective population sizes and living in a highly connected environment (Cowen & Sponaugle, 2009), they generally show low levels of genetic differentiation across their species ranges (Palumbi, 1992)
The principal component analysis clearly shows that the Chilean mussels (MAU) group with the Kerguelen mussels in accordance with them being both named M. platensis; while the Australasian samples (Australia, Tasmania and New-Zealand), usually named M. planulatus, cluster with the Northern M. galloprovincialis
We first analyzed the genetic relationship of the Southern Hemisphere Kerguelen mussels with the three Northern species (M. edulis, M. galloprovincialis and M. trossulus) at 1,269 contigs

Summary

Introduction

Marine species with planktonic larvae are high-dispersal organisms, with large effective population sizes and living in a highly connected environment (Cowen & Sponaugle, 2009), they generally show low levels of genetic differentiation across their species ranges (Palumbi, 1992). There is some evidence that micro-geographic genetic-environment associations occur at specific loci in marine species, such as barnacles (Schmidt & Rand, 1999), mussels (Koehn et al, 1980) or Atlantic killifishes (Reid et al, 2017), despite genome-wide genetic homogeneity These locus-specific associations are traditionally expected in regions of the species range where environmental gradients promote local adaptation of specific populations (Schmidt et al, 2008). The reduction in gene flow between genetic backgrounds is expected to be visible only on a subset of markers either because localized at an intermediate linkage map distance to reproductive isolation genes (Gagnaire et al, 2015) or because of heterogeneous differentiation produced by linked selection (Simon & Duranton, 2018) This potential effect of introgression on our capacity to detect connectivity breaks in apparently well-mixed populations is of central concern to conservation and species management (Gagnaire et al, 2015)

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