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.
a b s t r a c t a r t i c l e i n f oWorldwide, marine and coastal ecosystems are heavily invaded by introduced species and the potential role of parasites in the success and impact of marine invasions has been increasingly recognized. In this review, we link recent theoretical developments in invasion ecology with empirical studies from marine ecosystems in order to provide a conceptual framework for studying the role of parasites and their hosts in marine invasions. Based on an extensive literature search, we identified six mechanisms in which invaders directly or indirectly affect parasite and host populations and communities: I) invaders can lose some or all of their parasites during the invasion process (parasite release or reduction), often causing a competitive advantage over native species; II) invaders can also act as a host for native parasites, which may indirectly amplify the parasite load of native hosts (parasite spillback); III) invaders can also be parasites themselves and be introduced without needing co-introduction of the host (introduction of free-living infective stages); IV) alternatively, parasites may be introduced together with their hosts (parasite co-introduction with host); V) consequently, these co-introduced parasites can sometimes also infect native hosts (parasite spillover); and VI) invasive species may be neither a host nor a parasite, but nevertheless affect native parasite host interactions by interfering with parasite transmission (transmission interference). We discuss the ecological and evolutionary implications of each of these mechanisms and generally note several substantial effects on natural communities and ecosystems via i) mass mortalities of native populations creating strong selection gradients, ii) indirect changes in species interactions within communities and iii) trophic cascading and knock-on effects in food webs that may affect ecosystem function and services. Our review demonstrates a wide range of ecological and evolutionary implications of marine invasions for parasite-host interactions and suggests that parasite-mediated impacts should be integrated in assessing the risks and consequences of biological invasions.
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