Trans-Atlantic Distribution and Introgression as Inferred from Single Nucleotide Polymorphism: Mussels Mytilus and Environmental Factors

Abstract

Large-scale climate changes influence the geographic distribution of biodiversity. Many taxa have been reported to extend or reduce their geographic range, move poleward or displace other species. However, for closely related species that can hybridize in the natural environment, displacement is not the only effect of changes of environmental variables. Another option is subtler, hidden expansion, which can be found using genetic methods only. The marine blue mussels Mytilus are known to change their geographic distribution despite being sessile animals. In addition to natural dissemination at larval phase—enhanced by intentional or accidental introductions and rafting—they can spread through hybridization and introgression with local congeners, which can create mixed populations sustaining in environmental conditions that are marginal for pure taxa. The Mytilus species have a wide distribution in coastal regions of the Northern and Southern Hemisphere. In this study, we investigated the inter-regional genetic differentiation of the Mytilus species complex at 53 locations in the North Atlantic and adjacent Arctic waters and linked this genetic variability to key local environmental drivers. Of seventy-nine candidate single nucleotide polymorphisms (SNPs), all samples were successfully genotyped with a subset of 54 SNPs. There was a clear interregional separation of Mytilus species. However, all three Mytilus species hybridized in the contact area and created hybrid zones with mixed populations. Boosted regression trees (BRT) models showed that inter-regional variability was important in many allele models but did not prevail over variability in local environmental factors. Local environmental variables described over 40% of variability in about 30% of the allele frequencies of Mytilus spp. For the 30% of alleles, variability in their frequencies was only weakly coupled with local environmental conditions. For most studied alleles the linkages between environmental drivers and the genetic variability of Mytilus spp. were random in respect to “coding” and “non-coding” regions. An analysis of the subset of data involving functional genes only showed that two SNPs at Hsp70 and ATPase genes correlated with environmental variables. Total predictive ability of the highest performing models (r2 between 0.550 and 0.801) were for alleles that discriminated most effectively M. trossulus from M. edulis and M. galloprovincialis, whereas the best performing allele model (BM101A) did the best at discriminating M. galloprovincialis from M. edulis and M. trossulus. Among the local environmental variables, salinity, water temperature, ice cover and chlorophyll a concentration were by far the greatest predictors, but their predictive performance varied among different allele models. In most cases changes in the allele frequencies along these environmental gradients were abrupt and occurred at a very narrow range of environmental variables. In general, regions of change in allele frequencies for M. trossulus occurred at 8–11 psu, 0–10 °C, 60%–70% of ice cover and 0–2 mg m−3 of chlorophyll a, M. edulis at 8–11 and 30–35 psu, 10–14 °C and 60%–70% of ice cover and for M. galloprovincialis at 30–35 psu, 14–20 °C.

How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels

“…We have shown that this population is differentiated from both American, and South-European M. edulis, and appears as intermediate in the PCA ( Figure S2), Structure (Figures 2 and S5) and hybrid index analyses ( Figure 5). This observation previously made in Simon et al (2020), has recently been confirmed by Wenne et al (2020). Given its presence as the parental M. edulis population in the Øresund hybrid zone, and the complete absence of American ancestry in the Netherlands, the border between Southern and Northern European M. edulis probably falls somewhere near to the Danish coast (see also the previously observed differences between the North Sea and populations North of the Kattegat region; Stuckas, Stoof, Quesada, and Tiedemann, 2009).…”

“…(2020), has recently been confirmed by Wenne et al. (2020). Given its presence as the parental M. edulis population in the Øresund hybrid zone, and the complete absence of American ancestry in the Netherlands, the border between Southern and Northern European M. edulis probably falls somewhere near to the Danish coast (see also the previously observed differences between the North Sea and populations North of the Kattegat region; Bierne et al., 2003; Stuckas et al., 2009).…”

Musical Chairs on Temperate Reefs: Species Turnover and Replacement Within Functional Groups Explain Regional Diversity Variation in Assemblages Associated With Honeycomb Worms

“…Molecular identification was not attempted here, but could help resolve some of these taxonomic uncertainties in future work, as has been done for Mytilus spp. (Wenne et al, 2020). Similarly, nematodes were identified only to the phylum level, but did contribute significantly to the observed differences in assemblages between the Lusitanian and Lusitanian-Boreal regions.…”

“…However, due to the uncertainty regarding the morphological distinction at the species level between Mytilus edulis and Mytilus galloprovincialis, particularly at the juvenile stage (Jansen et al, 2007) and because hybridization occurs between the two (Daguin et al, 2001), all specimens sampled in the hybridization area (UK1, UK4, FR1, FR2, FR3, and FR4) were considered as Mytilus spp. (Wenne et al, 2020). All specimens are stored in the Laboratory of Coastal Benthic Ecology's collections at Ifremer (Plouzané, France).…”

Early detection of marine non-indigenous species on Svalbard by DNA metabarcoding of sediment

“…galloprovincialis and M. edulis/Mytilus trossulus, although M. edulis is so far the most abundant species (Mathiesen et al 2017;Węsławski and Kotwicki 2018). A recent study indicated that mussels (M. edulis) found on floating debris around Svalbard were hybrids of boreal and warm temperate taxa, some with genetic structure resembling populations in the UK, Iceland, and western mainland Europe (Wenne et al 2020). This shows the complex interpretation of origin that may also account for other NIS.…”