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

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.

Twin introductions by independent invader mussel lineages are both associated with recent admixture with a native congener in Australia

“…Estimates are also consistent with previous studies proposing separation times between northern and southern hemisphere Mytilus species ~0.5 to 1.3 million years ago based on mitochondrial loci (Gérard et al, ; Hilbish et al, ). More broadly, our findings support a scenario of parallel transequatorial migrations leading to the origins of southern hemisphere mussels, that is M. planulatus in Australasia which is more related to M. galloprovincialis (this study) and M. platensis in South America and the Kerguelen Islands which is more related to M. edulis in the northern hemisphere (Fraïsse, Haguenauer, et al, ). Under this scenario, however, mitochondrial introgression swamping following secondary contact between M. galloprovincialis and M. edulis (Fraïsse, Haguenauer, et al, ; Gérard et al, ) has been proposed to reconcile incongruent patterns of deep divergence at mitochondrial loci and reciprocal monophyly (with northern haplotypes) for all southern hemisphere lineages (Gérard et al, ).…”

“…In contrast, variation across the nuclear genomic background of Australian mussels alongside northern hemisphere taxa validated strong genetic affinities to M. galloprovincialis , suggesting a closer genetic relationship to the invasive taxon than implicated by mitochondrial loci (e.g. Fraïsse, Haguenauer, et al, ; Hilbish et al, ).…”

“…Gardner et al, ). A recent genetic survey has confirmed genomic differentiation between southern clades (Gérard et al, ), including the Kergulen islands; however, introgression with M. planulatus was not investigated (Fraïsse, Haguenauer, et al, ). The relationship between two southern Mytilus taxa (i.e.…”

“…To date, taxonomic delineation of the Australian endemic taxon has been hampered by a limited number of reliable loci that has also precluded detailed investigations of its recent evolutionary history. In particular, high levels of ancient incomplete lineage sorting among Mytilus species (resulting in various gene topologies) are likely to obscure signals of present day introgression and further amplify discordant species relationships when few loci are examined (Fraïsse, Haguenauer, et al, ). Thus, it remains unresolved (a) whether Australian native Mytilus comprise a lineage sufficiently divergent from northern M. galloprovincialis to warrant species status as M. planulatus , and (b) whether the history of Australian mussels reflects recent divergence only, or includes ongoing hybridization with introduced congeners.…”

Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

“…It should also be noted that independent contacts can show reversed associations with the environment, in agreement & Wenne, 2018; McDonald, Seed, & Koehn, 1991;Saarman & Pogson, 2015;Zbawicka, Trucco, & Wenne, 2018). By contrast, we only know of a few cases of M. edulis introductions -either transient or successful -into non-native areas (Casoli et al, 2016;Crego-Prieto et al, 2015;Fraïsse, Haguenauer, et al, 2018). Branch and Steffani (2004) reported that observed introductions of M. galloprovincialis happened close to large shipping ports, with a secondary range expansion from these points.…”