Quaternary geographical sibling speciation and population structuring in the Eastern Atlantic skates (suborder Rajoidea) Raja clavata and R. straeleni

Abstract

Running head: Allopatric cryptic speciation and population structuring in skates-2-ABSTRACT Aim Geographical (allopatric) speciation is a dynamic process whose footprints in the living world are a continuum of stages of increasing divergence. Geographical speciation can also contribute to the evolution of marine taxa. This study looked for two of these evolutionary stages (i.e. structured populations and sibling species) in the diversification patterns of two Atlantic skates (Raja, suborder Rajoidea) which exhibited high morphological and ecological conservativism. Location E Atlantic, Mediterranean, W Indian Methods Phylogeographical and population genetic analyses were performed by surveying DNA variation of 10 population samples assigned to the European Raja clavata and to the S African R. straeleni. Polymorphisms were detected by sequencing a mtDNA control region (CR) fragment and genotyping amplified fragment length polymorphism (AFLP) loci. Several statistical tests were used to explore genetic differentiation and population demography. Results CR haplotypes clustered in two clades consistent with taxon zoogeography. Mean sequence divergence between allopatric taxa amounted to 2% and Bayesian estimate of the time of the most recent common ancestor dated their separation between 0.155 and 1.3 Myr. Isolation-by-distance between European and S African demes was inferred from a significant correlation between coastal and genetic distances at AFLP loci. Null or low gene flow estimates suggested reproductive isolation between allopatric taxa. After separation, taxa have expanded moderately since 30-45 Kyr. Geographical subgrouping of CR haplotypes and significant genetic heterogeneity of samples at both markers featured the Atlantic and Mediterranean thornback skates, revealing pronounced levels of population structuring in this widely distributed taxon. Main conclusions In spite of the pronounced morpho-anatomical conservativism, R. clavata and R. straeleni are allopatric sibling species which diverged in the Pleistocene. A recent southward dispersal of European R. clavata-like elements along with the W African shelf with the budding of S African R. straeleni is ostensible. The tumultuous Quaternary palaeoclimatic history of equatorial and tropical Africa with the succession of glacial and interglacial palaeoenvironments could have promoted the repeated geographical isolation of local demes in relatively restricted refugial areas. Within the evolutionary trajectories experienced by Rajoidea, structured populations and allopatric sibling species could frequently represent intermediate frames of the microevolutionary animation proposed by Ernst Mayr to model allopatric speciation.

Resolving taxonomic uncertainty in vulnerable elasmobranchs: are the Madeira skate (Raja maderensis) and the thornback ray (Raja clavata) distinct species?

“…Raja clavata and R. straeleni are thought to have separated during the early Pleistocene as a result of glacial activity in equatorial Africa around 1.3 Ma. Using the highly variable CR, we calculated a mean sequence divergence of 1.8 % between these two species, which equals that demonstrated by Pasolini et al (2011). Similarly, the sequence divergence we calculated between R. clavata and the endemic Mediterranean skate R. radula (2.3 %) compares well to previous estimates used to date the evolution of R. radula to less than 5 million years ago (2.9 %, estimated from data from Valsecchi et al 2005).…”

“…Perhaps somewhat paradoxically, they are extremely morphologically conserved, maintaining a dorso-ventrally flattened body form typical of all batoids and brown-grey coloration. Despite evidence of speciation in the form of accumulated genetic differences (Pasolini et al 2011), species identification remains challenging, potentially due to the selection of a well-adapted phenotype (Futuyma 1979). In this study it was considered whether the endemic R. maderensis truly denotes an individual species or whether it represents a morphotype of the polytypic and widely distributed R. clavata.…”

“…New animal species most commonly evolve through allopatric speciation, which results from geographic isolation, beginning with highly structured populations (Coyne and Orr 2004;Gavrilets 2004). This had been suggested as the predominant mode of evolution in European skates (Pasolini et al 2011). Raja clavata and R. straeleni are thought to have separated during the early Pleistocene as a result of glacial activity in equatorial Africa around 1.3 Ma.…”

“…The thornback ray is distributed from Norway and Iceland to Northwest Africa, including the Mediterranean and Black Seas, and until recently was considered to inhabit waters as far south as southern Africa (Froese and Pauly 2011). The latter records most likely represented misidentifications of the recently diverged and morphologically similar biscuit skate, Raja straeleni, distributed in southern Africa (Pasolini et al 2011). Similarly, the rough ray (Raja radula), restricted to the Mediterranean (Morey et al 2009) is regarded as a sister species to R. clavata.…”

Genetic diversity and population structure of the red stingray, Dasyatis akajei inferred by AFLP marker

“…Based on the AFLP marker, investigation on genetic diversity of D. akajei populations presented a high level of Nei's index and the proportion of polymorphic loci in comparison with the current reported studies on elasmobranches (Pasolini et al, 2011). The result was compatible with the mtDNA-based estimates of a high level of haplotype diversity, which appeared to be a rare phenomenon for a species undergoing resource declining.…”