Parapatric genetic divergence among deep evolutionary lineages in the Mediterranean green crab, Carcinus aestuarii (Brachyura, Portunoidea, Carcinidae), accounts for a sharp phylogeographic break in the Eastern Mediterranean

Abstract

Background: Recently, population genetic studies of Mediterranean marine species highlighted patterns of genetic divergence and phylogeographic breaks, due to the interplay between impacts of Pleistocene climate shifts and contemporary hydrographical barriers. These factors markedly shaped the distribution of marine organisms and their genetic makeup. The present study is part of an ongoing effort to understand the phylogeography and evolutionary history of the highly dispersive Mediterranean green crab, Carcinus aestuarii (Nardo, 1847), across the Mediterranean Sea. Recently, marked divergence between two highly separated haplogroups (genetic types I and II) of C. aestuarii was discerned across the Siculo-Tunisian Strait, suggesting an Early Pleistocene vicariant event. In order to better identify phylogeographic patterns in this species, a total of 263 individuals from 22 Mediterranean locations were analysed by comparing a 587 basepair region of the mitochondrial gene Cox1 (cytochrome oxidase subunit 1). The examined dataset is composed of both newly generated sequences (76) and previously investigated ones (187).

Results: Our results unveiled the occurrence of a highly divergent haplogroup (genetic type III) in the most north-eastern part of the Mediterranean Sea. Divergence between the most distinct type III and the common ancestor of both types I and II corresponds to the Early Pleistocene and coincides with the historical episode of separation between types I and II. Our results also revealed strong genetic divergence among adjacent regions (separating the Aegean and Marmara seas from the remaining distribution zone) and confirmed a sharp phylogeographic break across the Eastern Mediterranean. The recorded parapatric genetic divergence, with the potential existence of a contact zone between both groups in the Ionian Sea and notable differences in the demographic history, suggest the likely impact of paleoclimatic events, as well as past and contemporary oceanographic processes, in shaping genetic variability of this species.

Conclusions: Our findings not only provide further evidence for the complex evolutionary history of the green crab in the Mediterranean Sea, but also stress the importance of investigating peripheral areas in the species' distribution zone in order to fully understand the distribution of genetic diversity and unravel hidden genetic units and local patterns of endemism.

Keywords: Biogeographic boundaries; Crustacea; Evolutionary history; Mediterranean Sea; Mitochondrial DNA; Population genetics.

Fig. 1

Sampling locations of the green crab Carcinus aestuarii across the Mediterranean Sea. Distribution patterns and proportions of Cox1 types (I, II, and III) along the examined locations are shown in couloured circles. S-T S: Siculo-Tunisian Strait; PHB: Peloponnese Hydrographic Break (represented by the quasi-circular anti-cyclonic feature southwest of Peloponnese). The base map was constructed with the software DIVA-GIS 7.5.0 (http://www.diva-gis.org)

Fig. 2

TCS haplotype network of Carcinus aestuarii, based on the alignment of 587 bp of the mitochondrial gene Cox1, showing the relationships among the recorded haplotypes. Haplotype 2 corresponds to the ancestral haplotype. Small black circles correspond to missing (or hypothetical) haplotypes. Each line between two points represents one mutational step. Circle sizes depict proportions of haplotypes; the smallest corresponds to 1 and the largest to 67 individuals

Fig. 3

Distribution patterns of types I, II and III of Carcinus aestuarii Cox1 gene across western and eastern Mediterranean basins (a) as well as geographic regions (b) (as defined in Table 1)

Fig. 4

Multidimensional scaling plot based on Φ_ST (Tajima-Nei distances) values between examined populations of Carcinus aestuarii

Fig. 5

Bayesian skyline plot for the two genetically defined groups of Carcinus aestuarii, as identified by SAMOVA; a: group 1; b: group 2. Populations, defining both geographic groups, are reported in the results and in Table 5 (K=2). BSP plots showing changes in effective population size (Ne) over time (measured in years before present). The thick solid line depicts the median estimate, and the margins of the blue area represent the highest 95% posterior density intervals