Cryptic diversity in smooth-shelled mussels on Southern Ocean islands: connectivity, hybridisation and a marine invasion

Abstract

Background Large numbers of endemic species inhabit subantarctic continental coasts and islands that are characterised by highly variable environmental conditions. Southern hemisphere populations of taxa that are morphologically similar to northern counterparts have traditionally been considered to be extensions of such Northern hemisphere taxa, and may not exhibit differentiation amongst geographically isolated populations in the Southern Ocean. Smooth-shelled blue mussels of the genus Mytilus that exhibit an anti-tropical distribution are a model group to study phylogeography, speciation and hybridisation in the sea, and contribute to the theory and practice of marine biosecurity. Methods We used a single nucleotide polymorphism (SNPs) panel that has the ability to accurately identify reference Northern and Southern hemisphere Mytilus taxa to test for evolutionary differentiation amongst native Southern Ocean island populations. Results Native mussels from the Falkland Islands and the Kerguelen Islands exhibited greatest affinity to native M. platensis d’Orbigny 1846 from the Atlantic coast of South America. The major Southern Ocean current flow from west to east is likely to explain the spreading of M. platensis to remote offshore islands, as adults via the process of rafting or perhaps directly as larvae. SNPs variation revealed that mussels from Tasmania were native and clearly differentiated from all other blue mussel groups in the Southern and Northern hemispheres. The native mussels M. planulatus from Tasmania and from mainland New Zealand (NZ), and tentatively M. aoteanus from the two NZ Southern Ocean offshore island groups (the Auckland Islands and Campbell Island), formed a distinct M. galloprovincialis –like Southern hemisphere group with closest affinity to Northern hemisphere M. galloprovincialis from the Mediterranean Sea. In all cases, the SNPs revealed evidence of hybridisation between two or more distinct taxa. The invasive Northern hemisphere M. galloprovincialis was identified only in Tasmania, amongst native mussels of a distinct Australian M. planulatus lineage. Conclusion Overall, our results reveal that Southern hemisphere island mussels have mixed genome ancestry and are native, not introduced by human activities. The preservation of distinct evolutionary lineages of Southern hemisphere species needs to be an ongoing focus of conservation efforts, given that population sizes on some of the remote offshore oceanic islands will be small and may be more easily adversely affected by invasion and subsequent hybridisation and introgression than larger populations elsewhere. Electronic supplementary material ...

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

“…A few samples used in our earlier works (ISLR in [17], ISLB and AZO in [61], BAR, ONE, LET and VIG in [21]) were genotyped with a set of single nucleotide polymorphisms (SNPs) for the purposes of this study. Except for these seven samples, results of genotyping with the same set of SNPs [25,26,37,38,62] were included in this study as shown in Table 1. Table 1 for definition of site abbreviations.…”

“…In general, M. trossulus is considered as the cold-water adapted species, M. edulis resides in temperate areas and M. galloprovincialis tolerates higher temperatures and has the most southerly native distribution of these three species in Europe in the Mediterranean and Black Sea. Moreover, M. galloprovincialis has successfully invaded temperate waters in other geographic areas such as South Africa, North and South America, Asia and Australia [37][38][39][40][41].…”

Some Examples of the Use of Molecular Markers for Needs of Basic Biology and Modern Society

“…However, in spite of the data on interspecies hybridization in some flatfish taxa [153], paraphyly even in this fish taxon generally seems attributable rather to the problem of weakness of traits under the morphological determination of individuals (and a habitat change impact in the latter case) than to the origin of the vast hybrid flock in the area of this study in the Baltic. However, such events cannot be ruled out, as it follows, for instance, from discussion in Section 2.2 and data for mussels [97,154].…”

“…Such signal comes from trees built for taxa of hybrid zones, as recently found for Mytilus ex. group edulis (e.g., [154,[163][164][165][166], etc.). In addition, complexes of rich tropical/near-tropical fauna give other examples of reticulations [86,167].…”

Development and Validation of a Multi-Locus PCR-HRM Method for Species Identification in Mytilus Genus with Food Authenticity Purposes

“…SI based in a single locus ("mono-locus") is relatively easy to perform, but this approach can produce conflicting results among markers and/or when individuals from hybrid zones are analyzed. Single nucleotide polymorphism (SNP) multi-locus panels have allowed for identifying M. edulis, M. galloprovincialis, M. trossulus [30,31], M. chilensis, M. planulatus and M. platensis [32][33][34]. However, genotyping a high number of SNPs may not be practical in routine analysis; therefore, it is attractive to develop reduced panels selecting highly informative SNPs for SI.…”