Genetic diversity and population structure of the rockpool shrimp Palaemon elegans based on microsatellites: evidence for a cryptic species and differentiation across the Atlantic–Mediterranean transition

Abstract

the rockpool shrimp Palaemon elegans is an ecologically important crustacean species within the european coastline fauna. in the present study, genetic diversity and population structure and connectivity were assessed by examining 21 polymorphic microsatellite loci at 13 sampling sites located along the natural distribution range. All localities showed similar levels of genetic variability. Significant deficits of heterozygosity were recorded, most likely due to the presence of null alleles. Genetic structure analyses revealed two clearly genetically distinct groups within P. elegans but without following any geographical or oceanographic basis. thus, our results provided nuclear evidence for the existence of a Mediterranean cryptic species within P. elegans, highlighting the need to revise its taxonomic status. Regarding P. elegans sensu stricto, population structuring was reported across the Atlantic-Mediterranean transition area, where the Almería-orán front restricts the gene flow between the Atlantic and the Mediterranean population. Moreover, while population connectivity was suggested between all Mediterranean localities, some substructure was found within the Atlantic group. Canary Islands exhibited a weak but significant genetic differentiation from all Atlantic mainland localities, consistent with the isolation-by-distance pattern detected throughout the Atlantic population. Overall, all these findings provided new insights into the population biology of P. elegans complex. The rockpool shrimp Palaemon elegans Rathke, 1837 is a crustacean decapod common in tidal rockpools, Zostera, Posidonia and Cymodocea sea grasses meadows and it also can be found in hypersaline lagoons and in slightly brackish water close to river mouths 1. This species is characterized by its capability to adapt to highly variable environments, as it can cope with a wide range of salinities, temperatures and oxygen conditions 2,3. Regarding to the native geographical distribution of P. elegans, it ranges from the eastern Atlantic Ocean (from Scotland and Norway to Mauritania, including the Azores, Madeira and Canary Islands) to the entire Mediterranean Sea and the Black Sea 4. Unintentional introductions resulted in this shrimp inhabiting the Caspian Sea and the Aral open

Mitogenome phylogenetics in the genus Palaemon (Crustacea: Decapoda) sheds light on species crypticism in the rockpool shrimp P. elegans

“…This genetic pattern was supported in later phylogeographic studies in the Mediterranean Sea also using mtDNA data [21,22]. Very recently, we have developed polymorphic microsatellite loci for this species [23] and accomplished a large analysis along its native distribution range that corroborated two clearly genetically distinct groups within P. elegans [13]. Our work strongly supported the existence of a cryptic and sympatric species within P. elegans in the Mediterranean Sea, providing nuclear evidence for the divergence signatures previously detected at mitochondrial level.…”

“…This work describes the mitochondrial genome of six Palaemon species for the first time, being one of them the cryptic species previously reported within P. elegans [12,13]. They are also the first European species of the genus Palaemon to have their mitogenome characterized.…”

“…The Mediterranean Sea has a tortuous geological history that largely contributed to its high level of biodiversity and endemism [71]. Specifically, it has been postulated that the MSC in late Miocene, [24] was the most likely scenario that gave rise of this cryptic species [12,13]. To further test this hypothesis, we used the MSC as calibration point for the mrca of P. elegans to estimate mitochondrial PCGs substitution rate in Palaemon and compare results to those attained in other pancrustacean species.…”

“…The ancestors of the cryptic species should survived in local refugia in the Mediterranean Sea during the MSC and diverged from Atlantic P. elegans. With the re-opening of the Strait of Gibraltar, the Mediterranean basin was rapidly flooded again with Atlantic water [77], so Atlantic P. elegans individuals were re-introduced, but they should no longer be able to reproduce with the cryptic species ancestors, since none genetic hybrids are currently detected [13]. The MSC was also considered the origin of other marine species, as crabs of the genera Carcinus [78] and Maja [79] or brittle stars of the genus Ophiothrix [69].…”

“…Regarding studies at the species level, phylogeographic analyses were conducted on several Palaemon species, detecting population structure in some of them that mainly corresponded to oceanographic discontinuities restricting gene flow. Presence of cryptic species was also pointed out in P. atrinubes, P. debilis, P. serrifer [9], P. vulgaris [11] and P. elegans [12,13]. Cryptic species occur when two or more genetically distinct molecular species (entities) were classified as a single nominal species because they are morphologically similar or indistinguishable [14,15].…”