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.

Keywords: Mytilus; North Atlantic; SNP; environmental variables; molecular population genetics.

Figure 1

Geographic location of 53 Mytilus spp. sampling sites. See Table 1 for definition of site abbreviations.

Figure 2

Neighbor-joining tree of 50 Mytilus populations based on the F_ST distance matrix from allele frequencies of the nucleotide polymorphism (SNP) loci. Population codes as shown in Table 1.

Figure 3

The first three axes of the correspondence analysis (CA) computed from the single nucleotide polymorphism (SNP) data on M. edulis from North Atlantic. Each point depicts a population.

Figure 4

Plot from STRUCTURE analysis at K = 4 showing group affinities of 53 study samples. Each individual (a) or population (b) is represented by a single vertical line representing mean q value for individual and within the sample. Names of the sample sites are shown below bar plots, black vertical lines separate the sample sites.

Figure 5

Frequency distribution of the score for a hybrid index giving the percentage of M. trossulus characteristic alleles. A score of zero is a pure M. edulis, whereas a score of one is a pure M. trossulus. Analysis was presented for four groups of populations: North America, North Russia, Scandinavia with Scotland and Baltic Sea. See Table 1 for definition and abbreviations.

Figure 6

Map of Mytilus lineages distribution in North Atlantics according to original and literature data (see the text for references). M. edulis is depicted by red (American lineage), yellow (West European lineage) and orange (North European M. edulis, the product of intermingling between American and West European lineages), M. trossulus by blue (the Baltic lineage by light blue), M. galloprovincialis by black (Mediterranean lineage) and green (Atlantic lineage).