Abstract
The regions of the Black, Caspian, and Azov seas are known for being both (i) the place of extensive crustacean radiation dated to the times of Paratethys and Sarmatian basins, and (ii) present donors of alien and invasive taxa to many areas worldwide. One amphipod morphospecies,Dikerogammarus haemobaphes, is known both as native to rivers draining to the Black and Caspian seas as well as a successful invader (nicknamed demon shrimp) in Central and Western European rivers. Based on mitochondrial (COI and 16S) and nuclear (28S) datasets and 41 sampling sites, representing both the native (19) and the invaded (22) range, we assessed cryptic diversity, phylogeography and population genetics of this taxon. First, we revealed the presence of two divergent lineages supported by all markers and all species delimitation methods. The divergence between the lineages was high (18.3% Kimura 2-parameter distance for COI) and old (ca. 5.1 Ma), suggesting the presence of two cryptic species withinD. haemobaphes. Lineage A was found only in a few localities in the native range, while lineage B was widespread both in the native and in the invaded range. Although genetic divergence within lineage B was shallow, geographic distribution of 16S and COI haplotypes was highly heterogeneous, leading us to the definition of four Geo-Demographic Units (GDUs). Two GDUs were restricted to the native range: GDU-B1 was endemic for the Durugöl (aka Duruşu) Liman in Turkey, whereas GDU-B2 occurred only in the Dniester River. GDU-B3 was both present in several localities in the native range in the Black Sea drainage area and widespread in Central and Western Europe. The GDU-B4 was found exclusively in the Moskva River in Russia. Extended Bayesian Skyline Plot indicated steady growth of GDU-B3 population size since 30 ka, pointing to the rather old history of its expansion, first in the late Pleistocene in the native range and nowadays in Central and Western Europe. The analysis of haplotype distribution across the present distribution range clearly showed two invasion routes to Central and Western Europe. The first one, originating from the lower Dnieper, allowed the demon shrimp to colonize Polish rivers and the Mittellandkanal in Germany. The second one, originating from the Danube delta, allowed to colonize the water bodies in the upper Danube basin. The UK population has originated from the Central Corridor, as only a haplotype found exclusively along this route was recorded in the UK. Population genetics analysis showed that the invasion of the demon shrimp along the Central Corridor was not associated with the loss of genetic diversity, which might contribute to the success of this invader in the newly colonized areas.
Highlights
Global climate changes impact the size and extent of areas that may potentially be inhabited by many species (Parmesan 2006)
In the dataset composed of 433 sequences, we identified 15 haplotypes of 16S (302 bp) and 27 haplotypes of c oxidase subunit I gene (COI) (598 bp)
The concatenation of both fragments (900 bp) resulted in the recognition of 39 mtDNA haplotypes derived from different combinations of the 16S and COI haplotypes (Suppl. material 2: Table S2, Suppl. material 3: Table S3)
Summary
Global climate changes impact the size and extent of areas that may potentially be inhabited by many species (Parmesan 2006). In the case of another well studied invasive amphipod, Dikerogammarus villosus, which had widely spread in Central and Western Europe from its native range in the PontoCaspian region, there was no evidence for presence of cryptic species and only two weakly divergent genetic lineages were found outside its native range (Wattier et al 2007; Rewicz et al 2015). Taking into account what is currently known about the recently studied and closely related killer shrimp, the history of the demon shrimp invasion and the geological history of the native area, we hypothesized that (i) it is plausible that in the native region the demon shrimp encompasses several weakly divergent lineages dating back to Pleistocene, (ii) there are possibly two sources, the Dnieper and the Danube deltas and, two independent routes for the species invasion to Central and Western Europe – the so-called Central Corridor and the Southern Corridor of invasion, respectively, (iii) learning from the invasion history of the closely related killer shrimp, we can expect that the populations of the demon shrimp will show signs of demographic and spatial expansion and no loss of genetic diversity, except the UK population, in comparison to the source population
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