rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi

Abstract

In Europe, the last 20 years have seen a spectacular increase in accidental introductions of marine species, but it has recently been suggested that both the actual number of invaders and their impacts have been seriously underestimated because of the prevalence of sibling species in marine habitats. The red alga Polysiphonia harveyi is regarded as an alien in the British Isles and Atlantic Europe, having appeared in various locations there during the past 170 years. Similar or conspecific populations are known from Atlantic North America and Japan. To choose between three competing hypotheses concerning the origin of P. harveyi in Europe, we employed rbcL sequence analysis in conjunction with karyological and interbreeding data for samples and isolates of P. harveyi and various congeners from the Pacific and North Atlantic Oceans. All cultured isolates of P. harveyi were completely interfertile, and there was no evidence of polyploidy or aneuploidy. Thus, this biological species is both morphologically and genetically variable: intraspecific rbcL divergences of up to 2.1% are high even for red algae. Seven rbcL haplotypes were identified. The four most divergent haplotypes were observed in Japanese samples from Hokkaido and south-central Honshu, which are linked by hypothetical 'missing' haplotypes that may be located in northern Honshu. These data are consistent with Japan being the centre of diversity and origin for P. harveyi. Two non-Japanese lineages were linked to Hokkaido and Honshu, respectively. A single haplotype was found in all North Atlantic and Mediterranean accessions, except for North Carolina, where the haplotype found was the same as that invading in New Zealand and California. The introduction of P. harveyi into New Zealand has gone unnoticed because P. strictissima is a morphologically indistinguishable native sibling species. The sequence divergence between them is 4-5%, greater than between some morphologically distinct red algal species. Two different types of cryptic invasions of P. harveyi have therefore occurred. In addition to its introduction as a cryptic sibling species in New Zealand, P. harveyi has been introduced at least twice into the North Atlantic from presumed different source populations. These two introductions are genetically and probably also physiologically divergent but completely interfertile.

Cryptic invasion drives phenotypic changes in central European threespine stickleback

“…The occurrence and impact of such invasions may however be underestimated in cases of cryptic invasions, i.e., when a native species becomes admixed or even genetically replaced by one or multiple distinct genetic lineages of the same species (Saltonstall 2002;Mabuchi et al 2008;Holsbeek et al 2008). Cryptic invasions are commonly unrecognized because the invaders are in many cases mistaken for native species (Saltonstall 2002;Mabuchi et al 2008), yet the invading lineage may differ from their native counterparts in their phenotype (Holsbeek et al 2008;Mackie et al 2012) and/ or physiology (McIvor et al 2001). Such phenotypic changes are however less often reported because relatively few cases exist where historical records are available to document phenotypic changes following a cryptic invasion (Wandeler et al 2007;Crispo et al 2011).…”

Patterns of genetic diversity of the cryptogenic red alga Polysiphonia morrowii (Ceramiales, Rhodophyta) suggest multiple origins of the Atlantic populations

“…2004), Neosiphonia harveyi (McIvor et al. 2001), Gracilaria vermiculophylla (Kim et al. 2010) have suggested that many widespread introductions may have originated from a particularly successful introduced population (corresponding to a restricted number of genotypes) rather than from genotypes representative of the native range (Lombaert et al.…”

Taxonomic reassessment ofPolysiphonia foetidissima(Rhodomelaceae, Rhodophyta) and similar species, includingP. schneideri, a newly introduced species in Europe

“…Stuercke & Freshwater, 2010). Likewise, some introduced species of Polysiphonia closely resemble native species and require molecular analyses to identify them reliably (McIvor et al, 2001;Geoffroy et al, 2012). In this regard, numerous introductions of macroalgae to the Atlantic European coasts have been reported over the past four decades (Farnham, 1980;Maggs & Stegenga, 1999;Hewitt et al, 2007;Bárbara et al, 2008;Couceiro et al, 2011;Mineur et al, 2012).…”

“…In this regard, numerous introductions of macroalgae to the Atlantic European coasts have been reported over the past four decades (Farnham, 1980;Maggs & Stegenga, 1999;Hewitt et al, 2007;Bárbara et al, 2008;Couceiro et al, 2011;Mineur et al, 2012). Moreover, the actual number of invaders and their impacts may have been seriously underestimated (McIvor et al, 2001). The only species of Polysiphonia sensu lato previously reported as introduced to the Atlantic Europe are Neosiphonia harveyi and P. morrowii from Atlantic North America and Japan, respectively (Maggs & Stegenga, 1999;McIvor et al, 2001).…”

“…Moreover, the actual number of invaders and their impacts may have been seriously underestimated (McIvor et al, 2001). The only species of Polysiphonia sensu lato previously reported as introduced to the Atlantic Europe are Neosiphonia harveyi and P. morrowii from Atlantic North America and Japan, respectively (Maggs & Stegenga, 1999;McIvor et al, 2001). Nonetheless, the challenges of species discrimination noted above suggest that other cases of cryptic introductions may have been overlooked within this difficult group.…”