Vicariance patterns in the Mediterranean Sea: east–west cleavage and low dispersal in the endemic seagrass Posidonia oceanica

Abstract

Aim The seagrass, Posidonia oceanica is a clonal angiosperm endemic to the Mediterranean Sea. Previous studies have suggested that clonal growth is far greater than sexual recruitment and thus leads to low clonal diversity within meadows. However, recently developed microsatellite markers indicate that there are many different genotypes, and therefore many distinct clones present. The low resolution of markers used in the past limited our ability to estimate clonality and assess the individual level. New high‐resolution dinucleotide microsatellites now allow genetically distinct individuals to be identified, enabling more reliable estimation of population genetic parameters across the Mediterranean Basin. We investigated the biogeography and dispersal of P. oceanica at various spatial scales in order to assess the influence of different evolutionary factors shaping the distribution of genetic diversity in this species. Location The Mediterranean. Methods We used seven hypervariable microsatellite markers, in addition to the five previously existing markers, to describe the spatial distribution of genetic variability in 34 meadows spread throughout the Mediterranean, on the basis of an average of 35.6 (± 6.3) ramets sampled. Results At the scale of the Mediterranean Sea as a whole, a strong east–west cleavage was detected (amova). These results are in line with those obtained using previous markers. The new results showed the presence of a putative secondary contact zone at the Siculo‐Tunisian Strait, which exhibited high allelic richness and shared alleles absent from the eastern and western basins. F statistics (pairwise θ ranges between 0.09 and 0.71) revealed high genetic structure between meadows, both at a small scale (about 2 to 200 km) and at a medium scale within the eastern and western basins, independent of geographical distance. At the intrameadow scale, significant spatial autocorrelation in six out of 15 locations revealed that dispersal can be restricted to the scale of a few metres. Main conclusions A stochastic pattern of effective migration due to low population size, turnover and seed survival is the most likely explanation for this pattern of highly restricted gene flow, despite the importance of an a priori seed dispersal potential. The east–west cleavage probably represents the outline of vicariance caused by the last Pleistocene ice age and maintained to this day by low gene flow. These results emphasize the diversity of evolutionary processes shaping the genetic structure at different spatial scales.

Evolutionary history of the seagrass genus Posidonia

“…Biogeographic surveys of genetic diversity in P. oceanica (Arnaud-Haond et al 2007, Serra et al 2010, based on microsatellite nuclear markers, confirmed strong cleavage between populations in the eastern and western Mediterranean basins probably resulting from vicariance events during the last glaciations. Although such isolation maintained over appropriate time scales could lead to speciation, these population divergence patterns still do not support speciation (Arnaud-Haond et al 2007, Serra et al 2010. The results from the present phylogenetic analysis also support the existence of a single Mediterranean species, P. oceanica, as no polymorphism was observed for 708 bp of the ITS throughout the entire Mediterranean Sea.…”

“…These observations led some investigators (Semroud et al 1992, Bussotti et al 1998) to question the taxonomic status of P. oceanica throughout the Mediterranean Sea. Biogeographic surveys of genetic diversity in P. oceanica (Arnaud-Haond et al 2007, Serra et al 2010, based on microsatellite nuclear markers, confirmed strong cleavage between populations in the eastern and western Mediterranean basins probably resulting from vicariance events during the last glaciations. Although such isolation maintained over appropriate time scales could lead to speciation, these population divergence patterns still do not support speciation (Arnaud-Haond et al 2007, Serra et al 2010.…”

“…Losos 2000) and dominance of clonal growth (Waycott et al 2006). Yet, genetic studies in populations of Cymodocea nodosa, Posidonia oceanica, Zostera noltii and Z. marina have reported high differentiation along their distributional ranges, although species-and site-dependent (Coyer et al 2004, Olsen et al 2004, Arnaud-Haond et al 2007, Alberto et al 2008. This indicates that large-scale dispersal as a general rule does not occur for seagrasses; therefore, unusual patterns of molecular evolution may have occurred and should be explored.…”

Scaling of processes shaping the clonal dynamics and genetic mosaic of seagrasses through temporal genetic monitoring

“…Numerous spatial studies have been carried out for diverse species, reporting highly variable levels of clonal richness that suggest a differential intensity between ISR and RSR strategies (Escaravage et al, 1998;Coyer et al, 2004;Olsen et al, 2004;Pluess and Stocklin, 2004;Diaz-Almela et al, 2007;Alberto et al, 2008). The extreme and most demonstrative cases of ISR dominance are the monoclonal meadows of some seagrass species, including Z. marina (Reusch et al, 1999;Olsen et al, 2004), C. nodosa (Alberto et al, 2008) or P. oceanica (Arnaud-Haond et al, 2007b. Meadows of the seagrass Z. marina surveyed simultaneously for their demographic evolution and genetic composition in Brittany were shown to be fluctuating mosaics of genetically differentiated patches with variable levels of genotypic and genetic diversity (Becheler et al, 2010).…”

Mapping the evolutionary twilight zone: molecular markers, populations and geography

“…Epperson (2005) reviewed how spatial autocorrelation analysis based on genetic variation among individuals within a local population can be used to estimate dispersal rates and other population parameters, and some attempts to link within-population patterns of spatial autocorrelation in genetic data to lifehistory traits have also been made (e.g. Degen et al, 2001;Arnaud-Haond et al, 2007). This can be important for improving predictions about population viability, which is critical for establishing optimum conservation strategies (e.g.…”