Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion

Abstract

Molecular approaches have proven efficient to identify cryptic lineages within single taxonomic entities. Sometimes these cryptic lineages maybe previously unreported or unknown invasive taxa. The genetic structure of the marine gastropod Stramonita haemastoma has been examined in the Western Mediterranean and North‐Eastern Atlantic populations with mtDNA COI sequences and three newly developed microsatellite markers. We identified two cryptic lineages, differentially fixed for alternative mtDNA COI haplogroups and significantly differentiated at microsatellite loci. The mosaic distribution of the two lineages is unusual for a warm‐temperate marine invertebrate with a teleplanic larval stage. The Atlantic lineage was unexpectedly observed as a patch enclosed in the north of the Western Mediterranean Sea between eastern Spain and the French Riviera, and the Mediterranean lineage was found in Macronesian Islands. Although cyto‐nuclear disequilibrium is globally maintained, asymmetric introgression occurs in the Spanish region where the two lineages co‐occur in a hybrid zone. A first interpretation of our results is mito‐nuclear discordance in a stable postglacial hybrid zone. Under this hypothesis, though, the location of genetic discontinuities would be unusual among planktonic dispersers. An alternative interpretation is that the Atlantic lineage, also found in Senegal and Venezuela, has been introduced by human activities in the Mediterranean area and is introgressing Mediterranean genes during its propagation, as theoretically expected. This second hypothesis would add an additional example to the growing list of cryptic marine invasions revealed by molecular studies.

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

“…This contrasts with genetic patterns from mitochondrial DNA, which found North American haplotypes to be subsampled from those found in European populations with no discernible divergence (Einfeldt & Addison, 2015; Einfeldt et al., 2014). Noncongruent patterns between mitochondrial and genomic DNA are expected due to recombination between nuclear markers but not mitochondrial sequences, consistent with patterns seen in more recently introduced species (Ayari et al., 2017; Jeffery et al., 2017). Divergence between Europe and North America may be in part due to rapid evolution of introduced populations, which can arise from neutral (e.g., Baker & Moeed, 1987; Shultz, Baker, Hill, Nolan, & Edwards, 2016) and selective (e.g., Colautti & Barrett, 2013; Huey, Gilchrist, Carlson, Berrigan, & Serra, 2000) processes and ultimately lead to reproductive isolation between introduced populations and their sources (e.g., Montesinos et al, 2012).…”

“…The native ranges of other introduced marine species often exhibit unexpected genetic patterns, which could potentially be explained by human patterns of human movement. For example, in the invasive green crab Carcinus maenas mitochondrial haplotypes typically found in the South of Spain have also been found in the UK (Darling et al, 2008), and an Atlantic lineage of the marine gastropod Stramonita haemastoma may potentially have been cryptically introduced to the Mediterranean, where it hybridizes with a Mediterranean lineage (Ayari et al., 2017). The degree of association with contemporary vectors of transport is unknown for many taxa, due to limited availability of vessel surveys and the challenges of correctly identifying small inconspicuous species across all their life stages (Haydar, 2012).…”

Persistence of phylogeographic footprints helps to understand cryptic diversity detected in two marine amphipods widespread in the Mediterranean basin

“…Deli et al, 2017;Pannacciulli et al, 2017;Weiss et al, 2017) as well as other invertebrates (i.e. Fernández et al, 2015;De Luca et al, 2016;El Ayari et al, 2017), our study provides arguably the first evidence for such high level of cryptic diversity with deep divergence and evolutionary history. Even though it is not as pronounced as in the freshwater congeners (i.e.…”

Looking for diversity in all the right places? Genetic diversity is highest in peripheral populations of the reef-building polychaete Sabellaria alveolata

“…Common haplotypes may have been maintained in separate refugia, leading to the apparent genetic similarity at opposite range edges. Alternatively, human-mediated introduction from northern to southern populations may explain this pattern, as has been proposed for some molluscs (Simon-Bouhet et al 2006;El Ayari et al 2017). Genetic diversity in this population in Morocco is also relatively high, and presents a profile of demographic expansion (high H rar , with negative and significant values of Tajima's D and Fu's F S ), which could indicate the existence of another refugium in the southern part of the distribution, which unfortunately remained unsampled in our study, along with populations on the Iberian Peninsula.…”