Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal

Abstract

Mitochondrial DNA sequence data for 295 individuals of the marine bivalve Macoma balthica (L.) were collected from 10 sites across the European distribution, and from Alaska. The data were used to infer population subdivision history and estimate current levels of gene flow. Inferred historical biogeography was expected to be congruent with colonization of the Atlantic Ocean from the Pacific Ocean after the opening of the Bering Strait 3.5 Ma. In addition, the last glacial maximum, about 18000 years ago, was expected to have been responsible for most of the present-day distribution of molecular variation within Europe, because the area must have been recolonized after confinement to France and the south of the British Isles during the last glacial maximum. Current gene flow was hypothesized to be high, because the larvae of M. balthica spend 2-5 weeks drifting in the water column. The geographical distribution of one highly diverged haplotype clade was found to be disjunct and was encountered exclusively in samples from the Baltic Sea and Alaska. A molecular clock calibration for marine bivalve cytochrome-c-oxidase I dates this clade as having split off from the other haplotypes 9.8-39 Ma. Multiple colonizations of the Atlantic Ocean from the Pacific by M. balthica may explain the strong differences found between Baltic Sea and other European populations of this species. The sympatric occurrence of the highly diverged mitochondrial lineages in western parts of the Baltic Sea points to secondary admixture. With the use of coalescent analysis, population divergence times for French vs. other non-Baltic European populations ('Atlantic population assemblage') were estimated at a minimum of about 110000 years ago, well before the last glacial maximum 18000 years ago. Signatures of population divergence of M. balthica that appear to have originated during the Pleistocene have thus survived the last glacial maximum. Some of the populations within the Atlantic assemblage are currently isolated, while others appear to be connected by gene flow. Apparently, populations of this species can remain highly subdivided in spite of the potential for high gene flow, implying that their population and evolutionary dynamics can be independent.

Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France

“…Such areas could have served as temporary refugia during the LGM (23-19 kya) where local diversification would have allowed for the separate evolution of the two most common haplotypes and from which animals have subsequently dispersed and intermingled. Potentially, small northern ice-free refugia could have existed in the northern North Sea area and in small localities along the coast of Scotland and Norway (Luttikhuizen et al, 2003). Additional sampling from these areas should confirm this.…”

Climate‐related changes in recruitment of the bivalve Macoma balthica

“…in French, Atlantic, and Baltic population assemblages), meaning that they are numerically and evolutionarily independent (Luttikhuizen et al 2003). More detailed analyses of quantitative and molecular traits revealed genetic differences between adult populations of M. balthica living in the western Wadden Sea and the adjacent North Sea (Luttikhuizen et al 2003b). Even if part of the larvae originate from neighboring areas (or are lost to such areas), this would not seriously distort the analysis because temporal patterns in bivalve recruitment and stock biomass are synchronous in the Dutch and German Wadden Sea (Beukema et al 2001).…”

Population structure and historical demography of the thorny skate (Amblyraja radiata, Rajidae) in the North Atlantic

“…In the North Atlantic, marine species (so far investigated) seem to follow a pre-LGM expansion model, e.g., the common goby (Gysels et al 2004), the Atlantic swordfish , the Atlantic bluefin tuna , Atlantic bigeye tuna (Martinez et al 2006), the red alga Palmeria palmata (Provan et al 2005), the brown alga Fucus serratus (Hoarau et al submitted), the bivalve Macoma balthica (Luttikhuizen et al 2003) and the estuarine fish, Ethmalosa fimbriata (Durand et al 2005); where the date of expansion was estimated at between 536,000 (for the common goby) and 128,000 years (for the red alga, Palmeria palmata). Thus, it is likely that highly mobile species and/or those able to shift in the subtidal fared better in the many glacial-interglacial periods.…”