Revisiting the phylogeography of Asellus aquaticus in Europe: insights into cryptic diversity and spatiotemporal diversification

Abstract

Summary Pleistocene glaciations affected the present‐day distribution and genetic diversity of animal species in Europe. Deep genetic subdivisions observed in European populations of the widespread freshwater isopod morphospecies, Asellus aquaticus, suggest the presence of putative cryptic species. We used the DNA barcodes of the cytochrome c oxidase subunit 1 (COI) gene combined with distance‐ and tree‐based methods of species delimitation as a rapid tool for assessing the number of distinct operational taxonomic units (OTUs) representing potential cryptic species. The spatial and demographic aspect of A. aquaticus distribution was also analysed. We generated a tentative temporal framework for diversification within the morphospecies provided by the molecular clock approach. Altogether, our study included 603 COI sequences from 147 populations from all over Europe and Asia Minor, including the already published data deposited in GenBank. The mtDNA‐based phylogenetic and OTU delimitation pattern was assessed with results of the nuclear data set analysis including the sequence data derived from this study and those previously submitted in GenBank. In total, 16 haplotypes of 28S rDNA were used representing all COI‐based OTUs and 53 localities. Our results show that A. aquaticus is a conglomerate of genetically distinct COI OTUs. One of the OTUs seems to correspond to the nominative subspecies of A. aquaticus aquaticus, recently redescribed from Sweden, and another with the recently described A. kosswigi. Most of the OTUs are probably of pre‐Pleistocene origin and have narrow ranges in southern Europe. A recent expansion, in both demographic and spatial terms, was revealed in one OTU, which is widely distributed in Europe and represents A. aquaticus aquaticus. This may be explained by the post‐glacial recolonisation processes. According to our data, this OTU probably emerged and initially diversified in the west Balkans in the Middle/Late Pliocene with several lineages surviving and diversifying through the Pleistocene glaciations and expanding during the interglacials. In some cases, our 28S data support the COI‐based OTUs and provide ample evidence for the existence of distinct OTUs, especially in mountainous and karst areas. However, other COI OTUs are not reciprocally monophyletic with respect to nuclear marker. This phylogenetic pattern can be interpreted predominantly as a result of incomplete sorting of nuclear lineages, potentially indicating an ongoing speciation process, but also as an effect of introgression resulting from secondary contact of formerly peripatric or allopatric mitochondrial lineages.

Chronic radiation exposure at Chernobyl shows no effect on genetic diversity in the freshwater crustacean, Asellus aquaticus thirty years on

“…The suggestion of IBD in the present study is in disagreement with previous work conducted by Verovnik et al, (2005) (Sworobowicz et al, 2015;Verovnik et al, 2005). This may explain the presence of IBD in the present study, as it is assumed limited gene flow would have occurred between enclosed, isolated populations.…”

“…The suggestion of IBD in the present study is in disagreement with previous work conducted by Verovnik et al, () who studied the mitochondrial DNA and 28s rDNA sequences of A. aquaticus at a continental scale and found no evidence of IBD. The present study focused largely on closed lake systems with limited connectivity (though Dvorische, Yanovsky Crawl, and Glubokoye are floodplain lakes of the Pripyat river which would have been connected historically), which is fundamental to structuring A. aquaticus populations given known limitations on dispersal capacity (Sworobowicz et al, ; Verovnik et al, ). This may explain the presence of IBD in the present study, as it is assumed limited gene flow would have occurred between enclosed, isolated populations.…”

Lasting through the ice age: The role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean

“…Evidence is available to suggest that, in various animal groups a large portion of the genetic structure and diversity at the family, genus, and even species level is of pre‐Pleistocene origin (e.g. Costedoat & Gilles, ; Makhrov & Boltov, ; Sworobowicz et al, ; Verovnik, Sket, & Trontelj, ). During the last 2.5 My, Pleistocene glaciations have recurrently turned vast parts of northern and central Europe into ice deserts, or areas of permafrost, covered by tundra, with small, isolated patches of woodland vegetation (Frenzel, Pécsi & Velichko, ; Ray & Adams, ; Figure ).…”

Long‐term within‐basin isolation patterns, different conservation units, and interspecific mitochondrial DNA introgression in an amphipod endemic to the ancient Lake Skadar system, Balkan Peninsula

“…Conservation units are populations or groups of populations that should be considered separately in conservation projects, for their high distinctiveness, e.g. Genetic diversity can be addressed at different scales, from the continental or even global scale, covering whole populations of widely distributed species (for example see Baselga et al, 2013;Mamos, Wattier, Burzyński, & Grabowski, 2016;Sworobowicz et al, 2015), down to local scales of one mountain chain/valley, river, or lake, occupied by species with small ranges inhabiting patchy habitats. In practice, they may be, for example, populations characterised by haplotypes of mitochondrial DNA, which belong to different monophyletic lineages (for review see Coates, Byrne, & Moritz, 2018).…”

“…Although there is an agreement that genetic diversity should be monitored to be saved and preserved to the highest possible degree, activities undertaken to improve its protection are still insufficient (Allendorf, Hohenlohe, & Luikart, 2010;Graudal et al, 2014;Laikre et al, 2009;Peñas, Barrios, Bobo-Pinilla, Lorite, & Martínez-Ortega, 2016;Schwartz et al, 2006). Genetic diversity can be addressed at different scales, from the continental or even global scale, covering whole populations of widely distributed species (for example see Baselga et al, 2013;Mamos, Wattier, Burzyński, & Grabowski, 2016;Sworobowicz et al, 2015), down to local scales of one mountain chain/valley, river, or lake, occupied by species with small ranges inhabiting patchy habitats. Such habitats are often a result of fragmentation of formerly continuously occupied environment (Leonardi et al, 2012),…”