Natural history and molecular evolution of demersal Mediterranean sharks and skates inferred by comparative phylogeographic and demographic analyses

Abstract

BackgroundThe unique and complex paleoclimatic and paleogeographic events which affected the Mediterranean Sea since late Miocene deeply influenced the distribution and evolution of marine organisms and shaped their genetic structure. Following the Messinian salinity crisis and the sea-level fluctuations during the Pleistocene, several Mediterranean marine species developed deep genetic differentiation, and some underwent rapid radiation. Here, we consider two of the most prioritized groups for conservation in the light of their evolutionary history: sharks and rays (elasmobranchs). This paper deals with a comparative multispecies analysis of phylogeographic structure and historical demography in two pairs of sympatric, phylogenetically- and ecologically-related elasmobranchs, two scyliorhinid catsharks (Galeus melastomus, Scyliorhinus canicula) and two rajid skates (Raja clavata, Raja miraletus). Sampling and experimental analyses were designed to primarily test if the Sicilian Channel can be considered as effective eco-physiological barrier for Mediterranean demersal sympatric elasmobranchs.MethodsThe phylogeography and the historical demography of target species were inferred by analysing the nucleotide variation of three mitochondrial DNA markers (i.e., partial sequence of COI, NADH2 and CR) obtained from a total of 248 individuals sampled in the Western and Eastern Mediterranean Sea as well as in the adjacent northeastern Atlantic Ocean. Phylogeographic analysis was performed by haplotype networking and testing spatial genetic differentiation of samples (i.e., analysis of molecular variance and of principal components). Demographic history of Mediterranean populations was reconstructed using mismatch distribution and Bayesian Skyline Plot analyses.ResultsNo spatial genetic differentiation was identified in either catshark species, while phylogeographic structure of lineages was identified in both skates, with R. miraletus more structured than R. clavata. However, such structuring of skate lineages was not consistent with the separation between Western and Eastern Mediterranean. Sudden demographic expansions occurred synchronously during the upper Pleistocene (40,000–60,000 years ago) in both skates and G. melastomus, likely related to optimal environmental conditions. In contrast, S. canicula experienced a slow and constant increase in population size over the last 350,000 years.DiscussionThe comparative analysis of phylogeographic and historical demographic patterns for the Mediterranean populations of these elasmobranchs reveals that historical phylogeographic breaks have not had a large impact on their microevolution. We hypothesize that interactions between environmental and ecological/physiological traits may have been the driving force in the microevolution of these demersal elasmobranch species in the Mediterranean rather than oceanographic barriers.

Barriers in a sea of elasmobranchs: Fromfishingfor populations to testing hypotheses in population genetics

“…The number of publications was highly skewed towards sharks (superorders Galeomorphii and Squalomorphii) with 137 studies covering 70 species, compared to skates and rays (superorder Batoidea) with 37 publications covering 32 species. Only one study included population structure of both shark and ray species (Ferrari et al, 2018). A total of 21 shark families belonging to six orders were covered by the literature with most studies focusing on the family Carcharhinidae.…”

Molecular Taxonomy and Diversification of Atlantic Skates (Chondrichthyes, Rajiformes): Adding More Pieces to the Puzzle of Their Evolutionary History

“…miraletus [Angola 2]’. This complicated Atlantic evolutionary scenario is further enriched by the northernmost lineage R. miraletus , occurring in the Mediterranean Sea and adjacent North Eastern Atlantic waters [ 33 ]. It was, however, not included in this study.…”

“…Genetic analyses of Eastern Atlantic and Mediterranean species of the genus Raja helped to clarify relationships among closely related taxa, e.g., the reproductive isolation between Raja clavata and R. straeleni [ 28 ], the taxonomic uncertainties between R. clavata and R. maderensis [ 29 ], the cryptic species complex of R. miraletus [ 30 ] and the relationship between the Mediterranean endemic skate R. polystigma and its sibling species R. montagui [ 31 ]. Moreover, multiple mitochondrial DNA (mtDNA) markers have been widely used to assess elasmobranch species diversity and phylogeography [ 32 , 33 ] and to estimate levels of divergence and phylogenetic relationships among taxa [ 34 , 35 , 36 ]. DNA barcoding using the mitochondrial cytochrome oxidase subunit I (COI) fragment [ 37 ] has been proven to be a reliable tool for species identification in elasmobranchs [ 38 , 39 , 40 , 41 ] and appears to be particularly suited to strengthening morphological taxonomy [ 42 , 43 , 44 , 45 ].…”

Strongly structured populations and reproductive habitat fragmentation increase the vulnerability of the Mediterranean starry rayRaja asterias(Elasmobranchii, Rajidae)

“…The geographical structuring of a few rajid species in the Mediterranean has been revealed by studies combining different genetic approaches (Chevolot et al, 2006; Pasolini et al, 2011; Frodella et al, 2016; Ferrari et al, 2018). All this evidence accounts for patterns of genetic differentiation and potential ecological/environmental factors driving natural history and micro‐evolution of Mediterranean skate populations, such as oceanographic fronts and discontinuities or palaeoclimatic changes (Ferrari et al, 2018).…”