Anthropocene invasion of an ecosystem engineer: resolving the history ofCorophium volutator(Amphipoda: Corophiidae) in the North Atlantic

Abstract

Resolving the natural histories of species is important for the interpretation of ecological patterns, as it provides evolutionary context for the interactions between organisms and their environment. Despite playing an integral role on the intertidal mudflats of the North Atlantic as an abundant food source for predators and as an ecosystem engineer that alters the soft sediment environment, no previous studies have provided empirical evidence to determine the biogeographical origin of the amphipod Corophium volutator. To resolve its status as introduced or indigenous in Europe and North America, we analyzed sequence data for two mitochondrial loci and two nuclear markers, aiming to determine whether the present range of C. volutator is the result of unresolved taxonomy, persistence in glacial refugia, natural trans‐Atlantic dispersal, or human‐mediated introduction. Our results demonstrate a reduced genetic diversity in North American populations that is a subsample of diversity in European populations, with coalescent analyses of mitochondrial and nuclear DNA supporting different models of multiple introductions from Europe to the Bay of Fundy and Gulf of Maine in North America. These results suggest that C. volutator was introduced to North America prior to the first surveys of local biota in the 20th Century, which has broad implications for interpretations of community and ecosystem interactions in the North Atlantic intertidal. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 288–304.

Genetic discontinuity in two high dispersal marine invertebrates in the northwest Atlantic

“…Two population genetic studies on mudflat species that lack planktonic larval development (Corophium volutator: Einfeldt and Addison 2013; Hediste diversicolor: Einfeldt et al 2014) suggest that there is little or no gene flow between the Bay of Fundy and the Gulf of Maine. Although these results are consistent with reduced connectivity across this major biogeographic break, both species were recently introduced from Europe and thus may show patterns of genetic subdivision arising from independent founder events (Einfeldt and Addison 2015). Investigating species with high dispersal potential (i.e., species with pelagic larva) will help assess the degree to which the biogeographic break between the Bay of Fundy and the Gulf of Maine is a general feature limiting connectivity throughout the region.…”

Species-Specific Effects on Ecosystem Functioning Can Be Altered by Interspecific Interactions

“…However, if populations of both species are reduced to low levels, then our microcosm experiment suggests that nutrient flux, and thus pelagic productivity, may consequently decline (Fig 3B). The risk of such collapses may be particularly great in the Northwest Atlantic, where populations of both species have recently been shown to consist of introduced subsets of European populations [55,56], whose low genetic diversity may make them highly vulnerable to environmental change [57,58]. …”

Historical human activities reshape evolutionary trajectories across both native and introduced ranges

“…Combined with a restricted natural dispersal ability of both species, geographic barriers are expected to facilitate genetic differentiation between populations reflecting isolation‐by‐distance (IBD; e.g., Bockelmann, Reusch, Bijlsma, & Bakker, 2003; Launey, Ledu, Boudry, Bonhomme, & Naciri‐Graven, 2002), vicariance (e.g., Exadactylos, Geffen, Panagiotaki, & Thorpe, 2003; Panova et al., 2011), and local adaptation (e.g., Butlin et al., 2014). Europe had persistent coastal refugia during the last glacial maximum 18,000 years BP, and both species have distinct mitochondrial lineages consistent with persistence in multiple refugia (Einfeldt & Addison, 2015; Einfeldt et al., 2014; Virgilio, Fauvelot, Costantini, Abbiati, & Backeljau, 2009). Throughout the Holocene, soft‐sediment habitat was fragmented along coastlines by regions of coarse sediment and rocky substrata, with major discontinuities between the British Isles and continental Europe (Andersen et al., 2018).…”

“…We focus on two intertidal invertebrates, the amphipod Corophium volutator (Pallas, 1766) and annelid Hediste diversicolor (Müller, 1776, previously Nereis diversicolor ), which inhabit soft‐sediment habitat in the Bay of Biscay, North, and Baltic Seas in Europe and the Gulf of Maine and Bay of Fundy in North America. Until recently, they were thought to be native in North America (for review, see Einfeldt & Addison, 2015; Einfeldt, Doucet, & Addison, 2014). Three main lines of evidence suggest they were once moved between Europe and North America in ballast sediments before sediment movement was reduced when water ballast was adopted: (a) these soft‐sediment dwelling intertidal invertebrates are abundant in Europe and North America, but are not reported in intermediate land masses (Iceland and Greenland) which are expected to be inhabited by natural colonizers (Ingolfsson, 1992); (b) genetic diversity in both species is consistent with North American populations representing a subsample from more diverse European populations (Einfeldt & Addison, 2015; Einfeldt et al., 2014); (c) they lack a pelagic phase, brood‐rear their young, and reside in shallow constructed burrows (Peer, Linkletter, & Hicklin, 1986; Scaps, 2002).…”

“…Until recently, they were thought to be native in North America (for review, see Einfeldt & Addison, 2015; Einfeldt, Doucet, & Addison, 2014). Three main lines of evidence suggest they were once moved between Europe and North America in ballast sediments before sediment movement was reduced when water ballast was adopted: (a) these soft‐sediment dwelling intertidal invertebrates are abundant in Europe and North America, but are not reported in intermediate land masses (Iceland and Greenland) which are expected to be inhabited by natural colonizers (Ingolfsson, 1992); (b) genetic diversity in both species is consistent with North American populations representing a subsample from more diverse European populations (Einfeldt & Addison, 2015; Einfeldt et al., 2014); (c) they lack a pelagic phase, brood‐rear their young, and reside in shallow constructed burrows (Peer, Linkletter, & Hicklin, 1986; Scaps, 2002). This is expected to impart limited natural long‐distance dispersal capabilities (via drifting, swimming, or oceanic rafting), as well as a strong association with sediments used in historical ballast, and a weak association with water ballast (Hewitt, Gollasch, & Minchin, 2009).…”