How did subterranean amphipods cross the Adriatic Sea? Phylogenetic evidence for dispersal–vicariance interplay mediated by marine regression–transgression cycles

Abstract

Aim Freshwater subterranean amphipods with low dispersal abilities are known from both sides of the impermeable barrier, the Adriatic Sea. We tested the hypothesis that historical marine regression–transgression cycles shaped the distribution patterns of subterranean amphipods through repeated cycles of dispersal and vicariance against the hypothesis that subterranean amphipods colonized both sides of the Adriatic Sea independently. Location Western Balkan Peninsula, Adriatic Sea Islands and Apennine Peninsula, Europe. Taxon Genus Niphargus, a clade of freshwater subterranean amphipods (Crustacea: Amphipoda). Methods The taxonomic structure of the studied clade was revised using unilocus species delimitation methods. The timeframe of cladogenetic events was inferred using a multi‐locus time‐calibrated phylogeny and compared to the main regression–transgression events in the Miocene and Pleistocene. The geographical origin of the studied clade, species range expansions and contractions, as well as vicariance events were assessed through modelling of historical biogeography. Results Subterranean amphipods of the genus Niphargus, found on both sides of the Adriatic Sea, form a monophylum. The reconstructions of ancestral ranges suggest that the clade emerged in the Balkan Peninsula, dispersed three times independently to the Apennine Peninsula and once back to the Balkans. Adriatic Islands were colonized multiple times, predominantly from the Balkan Peninsula. The dispersal–vicariance events correspond to historical regression–transgression cycles in Miocene and Pleistocene. Main conclusions Marine regression–transgression cycles apparently shaped the distribution patterns of subterranean amphipods while the alternative hypothesis received no support. The actual distribution of subterranean faunas apparently reflects old biogeographical events.

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“…Described from a cave in the Istrian peninsula, it is found in fresh and brackish water caves along the coast as well as on islands; Sket (1966) hypothesized that it is a 'limnic immigrant' that tolerates mixohaline waters. This hypothesis was confirmed in a recent paper on the phylogeny of transadriatic Niphargidae (Delić et al, 2020). According to the latter study, during the Messinian Salinity Crisis, i.e., approximately 5.9-5.3 Ma, the ancestor of N. hebereri likely spread from the Apennine peninsula (where closely related species such as N. ictus Karaman, 1985 from the Frasassi cave complex in Marche region are present) and colonized the Adriatic islands as well as the mainland of the Dinaric karst.…”

Molecular taxonomy, phylogeny and biogeography of the Niphargus tatrensis species complex (Amphipoda, Niphargidae) in Austria

“…In the first place, the subterranean habitats are difficult to access (especially caves, which may require advanced speleological techniques), most species have restricted distribution ranges (although exceptions exist: Fišer et al 2010;Copilaş-Ciocianu et al 2018) and sometimes species are known from single or few localities difficult to trace using old taxonomic literature and museum labels. Second, the morphotaxonomy of this group is very unsatisfactory (Fišer et al 2008;): morphological characters are highly homoplastic (Fišer et al 2008(Fišer et al , 2010, and differences between species are weak while intraspecific variation can be high (Delić et al 2020), requiring the examination of an unpractically large, usually unattainable number of specimens from each locality. Although molecular techniques have been found to be powerful tools for complementing the traditional morphotaxonomy of Niphargus (Flot 2010, Brad et al 2015, a number of shortcomings may cast a shadow on the taxonomic value of recent molecular revisions: (i) a lack of sequences obtained from topotypic specimens, (ii) identification errors in attributing sequences to the described morphospecies, (iii) chromatograms of low quality and/or improperly basecalled (notably in case of heterozygous individuals) and (iv) an uncritical use of species delimitation methods in describing cryptic species, considering that they can yield different results, especially if based on single loci Flot 2015, 2018).…”

Cave amphipods reveal co‐variation between morphology and trophic niche in a low‐productivity environment

“…Morphological identification was further supported by DNA barcoding using the cytochrome oxidase I gene in three species, following protocols from Delić et al. (2020). Two of the collected Niphargus species were not formally described: Niphargus sp.…”

“…Finally, we tested whether the gnathopod size and shape correlated with the TP and food resources, while accounting for phylogenetic relationships among species. We used the latest published Niphargus phylogeny, from which we pruned irrelevant species (details on phylogeny reconstruction available in Delić et al., 2020; full phylogeny is available in Figure S1). To account for phylogenetic uncertainty, we extracted 1,000 random trees out of 120,000 trees from the stationary phase of two Markov chains Monte Carlo runs in Bayesian phylogenetic analysis.…”

“…Third, Niphargus species feed on diverse food resources, including decaying plant material, detritus, and carcasses, but also exhibit active predatory behavior (Ercoli et al., 2019; Fišer et al., 2010; Pacioglu et al., 2020), including cannibalism (Luštrik et al., 2011; Sket, 1958). Finally, the well‐established phylogeny of Niphargus (Delić et al., 2020) enables us to test for trait‐function relationships while accounting for statistical error stemming from phylogenetic relatedness.…”