Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification

Abstract

Current theory predicts that a shift to a new habitat would increase the rate of diversification, while as lineages evolve into multiple species, intensified competition would decrease the rate of diversification. We used Holarctic amphipods of the genus Gammarus to test this hypothesis. We sequenced four genes (5,088 bp) for 289 samples representing 115 Gammarus species. A phylogenetic analysis showed that Gammarus originated from the Tethyan region with a saline ancestry in the Paleocene, and later colonized the freshwater habitat in the Middle Eocene. Ancestral range reconstruction and diversification mode analysis combined with paleogeological and paleoclimatic evidence suggested that the habitat shift from saline to freshwater led to an increased diversification rate. The saline lineage of Gammarus dispersed to both sides of the Atlantic at 55 million years ago (Ma), because of the few barriers between the Tethys and the Atlantic, and diversified throughout its evolutionary history with a constant diversification rate [0.04 species per million years (sp/My)]. The freshwater Gammarus, however, underwent a rapid diversification phase (0.11 sp/My) until the Middle Miocene, and lineages successively diversified across Eurasia via vicariance process likely driven by changes of the Tethys and landmass. In particular, the freshwater Gammarus lacustris and Gammarus balcanicus lineages had a relatively high diversification shift, corresponding to the regression of the Paratethys Sea and the continentalization of Eurasian lands during the Miocene period. Subsequently (14 Ma), the diversification rate of the freshwater Gammarus decreased to 0.05 and again to 0.01 sp/My. The genus Gammarus provides an excellent aquatic case supporting the hypothesis that ecological opportunities promote diversification.evolution | molecular dating | range expansion

Zoogeography of epigean freshwater Amphipoda (Crustacea) in Romania: <br />fragmented distributions and wide altitudinal variability

“…Two of them, G. balcanicus dacicus Dobreanu & Manolache, 1942 and G. balcanicus montanus S. Karaman, 1929, were formally described as subspecies. The third morph resembles G. balcanicus from the type locality (Cărăuşu et al 1955), but the results of Hou et al (2011) and Mamos et al (2014) indicate that the Romanian populations are molecularly distinct from those from the type locality and, therefore, we label it G. cf. balcanicus.…”

“…At present it is known that G. balcanicus, G. fossarum, G. komareki, G. roeselii, and G. pulex are taxonomically challenging poly/ paraphyletic cryptic species complexes (indicated by "s.l." below) (Scheepmaker 1990;Müller 1998;Hou et al 2011Hou et al , 2013Weiss et al 2013). We are aware that the Romanian populations might represent distinct cryptic lineages, as has been shown for G. balcanicus (Hou et al 2011.…”

“…below) (Scheepmaker 1990;Müller 1998;Hou et al 2011Hou et al , 2013Weiss et al 2013). We are aware that the Romanian populations might represent distinct cryptic lineages, as has been shown for G. balcanicus (Hou et al 2011. Without a detailed insight based on molecular data, we treated the Romanian populations as belonging to the above mentioned morphospecies.…”

“…balcanicus. Although both above-mentioned subspecies are presently synonymized with G. balcanicus (G. Karaman & Pinkster 1987), it seems likely that many such synonymized taxa might actually be distinct species (Hou et al 2011, Wysocka et al 2014. Thus, we considered it appropriate to show the morphology and distribution of the Romanian morphs of G. balcanicus separately, to facilitate future taxonomic and systematic studies.…”

“…Freshwater amphipod crustaceans are particularly suitable for biogeographical studies because of their restricted dispersal capabilities and the fragmentary nature of freshwater habitats (Väinölä et al 2008;Hou et al 2011). Amphipods are predominantly aquatic benthic animals that do not possess free-swimming larval stages or resistant propagules, and thus are prone to genetic differentiation and isolation (J.L.…”