Population genetic structure in Sabatieria (Nematoda) reveals intermediary gene flow and admixture between distant cold seeps from the Mediterranean Sea

Abstract

Background: There is a general lack of information on the dispersal and genetic structuring for populations of small-sized deep-water taxa, including free-living nematodes which inhabit and dominate the seafloor sediments. This is also true for unique and scattered deep-sea habitats such as cold seeps. Given the limited dispersal capacity of marine nematodes, genetic differentiation between such geographically isolated habitat patches is expected to be high. Against this background, we examined genetic variation in both mitochondrial (COI) and nuclear (18S and 28S ribosomal) DNA markers of 333 individuals of the genus Sabatieria, abundantly present in reduced cold-seep sediments. Samples originated from four Eastern Mediterranean cold seeps, separated by hundreds of kilometers, and one seep in the Southeast Atlantic.

Results: Individuals from the Mediterranean and Atlantic were divided into two separate but closely-related species clades. Within the Eastern Mediterranean, all specimens belonged to a single species, but with a strong population genetic structure (Φ_ST = 0.149). The haplotype network of COI contained 19 haplotypes with the most abundant haplotype (52% of the specimens) shared between all four seeps. The number of private haplotypes was high (15), but the number of mutations between haplotypes was low (1-8). These results indicate intermediary gene flow among the Mediterranean Sabatieria populations with no evidence of long-term barriers to gene flow.

Conclusions: The presence of shared haplotypes and multiple admixture events indicate that Sabatieria populations from disjunct cold seeps are not completely isolated, with gene flow most likely facilitated through water current transportation of individuals and/or eggs. Genetic structure and molecular diversity indices are comparable to those of epiphytic shallow-water marine nematodes, while no evidence of sympatric cryptic species was found for the cold-seep Sabatieria.

Fig. 1

Map of the location of the investigated cold seeps and distances between them. Amsterdam MV, Amon MV, Cheops and PM in the Eastern Mediterranean area; REGAB in the Atlantic Ocean. Source maps: http://www.geography-site.co.uk; http://www.emersonkent.com/map_archive/eastern_mediterranean.htm

Fig. 2

Phylogenetic ML tree of the COI haplotype sequences with indication of two clades. EM = Eastern Mediterranean clade; REG = REGAB clade. Values along branches are bootstrap values from the NJ algorithm based on p-distance and the ML procedure based on HKY + G, separated by a comma. Bootstrap values lower than 70 are not visualized in the figure. Each organism received a unique identification code (PCR code_Cold seep(s)_haplotype). In case haplotypes occurred at only one geographical location, their origin is indicated by a symbol and color (see legend). Haplotypes shared among several locations are not marked

Fig. 3

Phylogenetic ML trees for (a) 18S and (b) the D2D3 marker of 28S. EM: Eastern Mediterranean clade; REG: REGAB clade. Values along branches are bootstrap values of both NJ (p-distance) and ML (TrN + G) procedures, separated by a comma. Bootstrap values lower than 70 are not visualized in the figure. Each organism received a unique identification code (PCR code_Cold seep_haplotype). Symbols and colors indicate the origin of the sequences

Fig. 4

TCS network constructed with the haplotypes found in the EM clade. Each circle represents a haplotype, while the different colors represent the cold seeps. The division and size of the circles shows the frequency of this haplotype in each cold seep. Hatch marks along connecting branches indicate the number of substitutions between two haplotypes. Small black circles represent missing haplotypes