The role of isolation on contrasting phylogeographic patterns in two cave crustaceans

Abstract

BackgroundThe underlying mechanisms and processes that prompt the colonisation of extreme environments, such as caves, constitute major research themes of evolutionary biology and biospeleology. The special adaptations required to survive in subterranean environments (low food availability, hypoxic waters, permanent darkness), and the geographical isolation of caves, nominate cave biodiversity as ideal subjects to answer long-standing questions concerning the interplay amongst adaptation, biogeography, and evolution. The present project aims to examine the phylogeographic patterns exhibited by two sympatric species of surface and cave-dwelling peracarid crustaceans (Asellus aquaticus and Niphargus hrabei), and in doing so elucidate the possible roles of isolation and exaptation in the colonisation and successful adaptation to the cave environment.ResultsSpecimens of both species were sampled from freshwater hypogean (cave) and epigean (surface) habitats in Hungary, and additional data from neighbouring countries were sourced from Genbank. Sequencing of mitochondrial and nuclear loci revealed, through haplotype network reconstruction (TCS) and phylogenetic inference, the genetic structure, phylogeographic patterns, and divergence-time estimates of A. aquaticus and N. hrabei surface and cave populations. Contrasting phylogeographic patterns were found between species, with A. aquaticus showing strong genetic differentiation between cave and surface populations and N. hrabei lacking any evidence of genetic structure mediated by the cave environment. Furthermore, N. hrabei populations show very low levels of genetic differentiation throughout their range, which suggests the possibility of recent expansion events over the last few thousand years.ConclusionsIsolation by cave environment, rather than distance, is likely to drive the genetic structuring observed between immediately adjacent cave and surface populations of A. aquaticus, a predominantly surface species with only moderate exaptations to subterranean life. For N. hrabei, in which populations exhibit a fully ‘cave-adapted’ (troglomorphic) phenotype, the lack of genetic structure suggests that subterranean environments do not pose a dispersal barrier for this surface-cave species.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1094-9) contains supplementary material, which is available to authorized users.

Developmental Transcriptomic Analysis of the Cave-Dwelling Crustacean, Asellus aquaticus

“…Additionally, now that methods are established to investigate differential expression and allele-specific expression in embryonic samples of cave versus surface morphs of Asellus aquaticus, one next step is to expand the analysis to other cave populations. One of the advantages of working with this species is the number of populations that are thought to be independently evolved [24,60]. By examining gene expression and allele expression differences in these different cave populations, it should be possible to better understand how these cave-specific traits have evolved and determine if the independently evolved populations have evolved similarly or differently.…”

At the confluence of vicariance and dispersal: Phylogeography of cavernicolous springtails (Collembola: Arrhopalitidae, Tomoceridae) codistributed across a geologically complex karst landscape in Illinois and Missouri

“…With cave organisms, the majority of research studies have been limited to single species (e.g., Dörge, Zaenker, Klussmann‐Kolb, & Weigand, ; Faille et al., ) or cryptic species complexes with allopatric distributions (e.g., Gómez et al., ; Rastorgueff, Chevaldonné, Arslan, Verna, & Lejeusne, ). Few studies have incorporated phylogeographic approaches that consider intrinsic differences among codistributed cave‐dwelling species (see Pérez‐Moreno, Balázs, Wilkins, Herczeg, & Bracken‐Grissom, ; Weckstein et al., ).…”

“…Few studies have incorporated phylogeographic approaches that consider intrinsic differences among codistributed cave-dwelling species (see Pérez-Moreno, Balázs, Wilkins, Herczeg, & Bracken-Grissom, 2017;Weckstein et al, 2016).…”

“…Because troglobiotic and eutroglophilic springtails can be codistributed (Katz et al, 2016;Soto-Adames & Taylor, 2013), extrinsic evolutionary processes are likely exerting similar selective pressures upon them. Therefore, opposing patterns of genetic structure among these species distributed across the same geographic area can reflect intrinsic factors, such as differences in the degree of ecological association with cave habitats (cave dependence) that can affect a species' capacity to disperse across geographic barriers (Pérez-Moreno et al, 2017;Weckstein et al, 2016). Disparate geographic distributions among closely related surface springtails provide some indirect evidence that varying dispersal capacity may be associated with differences in species-specific traits (Costa et al, 2013;Katz, Giordano, & Soto-Adames, 2015), and Christiansen and Culver's (1987) biogeographic study of cave springtails revealed that more pronounced troglomorphy can be correlated with smaller geographic ranges.…”

Population divergence in aggregation and sheltering behaviour in surface and cave-adapted Asellus aquaticus (Crustacea: Isopoda)

“…The Molnár János Cave (47.518° N, 19.03608° E) is a water-filled cave of hydrothermal origin with a water temperature of 23-24 °C all year round. Despite the absence of physical barriers, the population inhabiting the Molnár János Cave has been genetically isolated from surface populations (including the Malom Lake population, see below) for at least 60 000 years and it shows the aforementioned troglomorphic adaptations (Pérez-Moreno et al 2017). The only available food source for this cave population of A. aquaticus is endogenous bacterial mats, visible organic material from the surface does not enter the cave (personal observation).…”