Glacial history of the European marine mussels Mytilus, inferred from distribution of mitochondrial DNA lineages

Abstract

Mussels of the genus Mytilus have been used to assess the circumglacial phylogeography of the intertidal zone. These mussels are representative components of the intertidal zone and have rapidly evolving mitochondrial DNA, suitable for high resolution phylogeographic analyses. In Europe, the three Mytilus species currently share mitochondrial haplotypes, owing to the cases of extensive genetic introgression. Genetic diversity of Mytilus edulis, Mytilus trossulus and Mytilus galloprovincialis was studied using a 900-bp long part of the most variable fragment of the control region from one of their two mitochondrial genomes. To this end, 985 specimens were sampled along the European coasts, at sites ranging from the Black Sea to the White Sea. The relevant DNA fragments were amplified, sequenced and analyzed. Contrary to the earlier findings, our coalescence and nested cladistics results show that only a single M. edulis glacial refugium existed in the Atlantic. Despite that, the species survived the glaciation retaining much of its diversity. Unsurprisingly, M. galloprovincialis survived in the Mediterranean Sea. In a relatively short time period, around the climatic optimum at 10 ky ago, the species underwent rapid expansion coupled with population differentiation. Following the expansion, further contemporary gene flow between populations was limited. Heredity (2014) 113, 250-258; doi:10.1038/hdy.2014.23; published online 12 March 2014 INTRODUCTION Sea mussels of the Mytilus edulis species complex, which consists of three subspecies: M. edulis, Mytilus trossulus, and Mytilus galloprovincialis, are widespread in northern and southern hemispheres (Gérard et al., 2008). All three taxa occur in the coastal water ecosystems surrounding Europe (Gosling, 1992). In Europe, M. trossulus prefers lower salinity waters: it has been identified in the Baltic Sea (Väinölä and Hvilsom, 1991), in Norwegian fjords (Ridgway and Naevdal, 2004), in Scotland (Beaumont et al., 2008), and in the Barents Sea (Väinölä and Strelkov, 2011). Single individuals possessing M. trossulus alleles were found in the Netherlands (Śmietanka et al., 2004). M. edulis ranges from the White Sea and the Barents Sea in the north, through the Atlantic coastal waters to southern France in the south. The range of M. galloprovincialis extends from the Azov and the Black Sea to the British Isles. In the areas where two subspecies coexist, hybridization has been observed. Two well-documented hybridization areas between M. edulis and M. trossulus exist in European waters. The first one extends from the Danish Straits into the Baltic Sea up to the Aland Islands, and the second has recently been discovered in Scotland (Beaumont et al., 2008). A strong, unidirectional genetic introgression from M. edulis to M. trossulus has been observed in the Baltic Sea area (Kijewski et al., 2006). The extreme effect is visible at the mitochondrial DNA (mtDNA) level, for the native M. trossulus mtDNA was replaced by M. edulis mitochondrial genome (Rawson and Hilbish, 1998). Wit...

Genetic diversity and connectivity within Mytilus spp. in the subarctic and Arctic

“…In general, F ST values between samples from Norway, Svalbard, and Russia and the Icelandic sample are lower than between the Icelandic sample and Greenlandic samples. Śmietanka, Burzyński, Hummel, and Wenne () suggested a single glacial Atlantic refugium founding European M. edulis . However, our studied sample from Iceland suggests the population to consist of individuals of mixed ancestry.…”

Massive gene presence/absence variation in the mussel genome as an adaptive strategy: first evidence of a pan-genome in Metazoa

“…The Mytilus genus has a complex evolutionary history, characterized by extensive gene flow among congeneric species, a process which is still ongoing in mosaic hybrid zones (42)(43)(44). However, the analysis of nuclear and mitochondrial genetic markers ruled out the possibility that our resequenced individuals were hybrids between M. galloprovincialis and other Mytilus species (Supplementary Data Note 7), which suggest that dispensable genes are unlikely to be recently introgressed allelic variants that cannot be mapped to the reference genome due to their sequence divergence (Supplementary Data Note 9).…”

A first report on coexistence and hybridization of Mytilus trossulus and M. edulis mussels in Greenland

“…The M. edulis species complex consists of three morphologically similar congeners: M. edulis, M. trossulus and M. galloprovincialis. Recently research has been intensified on the distribution of the species complex (e.g., Moreau et al 2005;Shields et al 2008;Riginos and Henzler 2008;Smietanka et al 2009;Stuckas et al 2009;Zbawicka et al 2012;Smietanka et al 2013Smietanka et al , 2014Zbawicka et al 2014), which evidently reflects a history of inter-and transoceanic dispersal, secondary contact and hybridization, besides the effect brought about by human activities (Väi-nölä and Strelkov 2011). It is thought that the complex originated from M. trossulus in the Pacific followed by colonization in the Northern Atlantic giving rise to both M. edulis and M. galloprovincialis (Vermeij 1992;Riginos and Cunningham 2005).…”