Cryptic diversity and mtDNA phylogeography of the invasive demon shrimp, Dikerogammarus haemobaphes (Eichwald, 1841), in Europe

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 within D. 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.

Successful post-glacial colonization of Europe by single lineage of freshwater amphipod from its Pannonian Plio-Pleistocene diversification hotspot

“…Amphipod crustaceans are listed among the richest in the number of invasive species successfully colonizing large water bodies (rivers and lakes) in Europe 40 , 41 . The prominent examples are Dikerogammarus villosus (Sowinsky, 1894) 40 , Dikerogammarus haemobaphes 42 and Pontogammarus robustoides (G.O. Sars, 1894) 39 .…”

Wide geographic distribution of overlooked parasites: Rare Microsporidia in Gammarus balcanicus, a species complex with a high rate of endemism

“…They are pathogenic to their two typical gammarid hosts ( D. villosus and D. haemobaphes , respectively) and use mainly horizontal transmission ( Ovcharenko et al, 2010 ; Bojko et al, 2015 , 2017 ). Since D. villosus and D. haemobaphes are invasive throughout Europe ( Rewicz et al, 2015 ; Jażdżewska et al, 2020 ) and carry pathogens during the invasion process ( Wattier et al, 2007 ; Bojko et al, 2019 ), their Microsporidian parasites have the potential to shift hosts and threaten local gammarid species ( Bacela-Spychalska et al, 2012 ; Bojko et al, 2019 ). The scattered infection of C. dikerogammari in G. balcanicus suggests that these infections could have been acquired by interspecific horizontal transfers at sympatric sites after contact with D. villosus ; however, no sites are known where G. balcanicus and D. villosus currently live in sympatry, and given their ecological requirements such a situation is highly improbable.…”

Distribution pattern of the brackish Apocorophium lacustre (Vanhoffen, 1911) (Amphipoda: Corophiidae) and the structure of the amphipod assemblages in the upper Oder River catchment

“…Such a scenario was observed in the Oder and Vistula rivers where the populations of D. haemobaphes were abundant. However, soon after, the appearance of the D. villosus began to decline (summarized by Jazdzewska et al, 2020), even if, in some conditions, those two species may coexist (Borza et al, 2017). On the contrary, C. curvispinum may regain this area and coexist with A. lacustre .…”