Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era

Abstract

Cave animals have historically attracted the attention of evolutionary biologists because of their bizarre 'regressive' characters and convergent evolution. However, understanding of their biogeographic and evolutionary history, including mechanisms of speciation, has remained elusive. In the last decade, molecular data have been obtained for subterranean taxa and their surface relatives, which have allowed some of the classical debates on the evolution of cave fauna to be revisited. Here, we review some of the major studies, focusing on the contribution of phylogeography in the following areas: biogeographic history and the relative roles of dispersal and vicariance, colonization history, cryptic species diversity and modes of speciation of cave animals. We further consider the limitations of current research and prospects for the future. Phylogeographic studies have confirmed that cave species are often cryptic, with highly restricted distributions, but have also shown that their divergence and potential speciation may occur despite the presence of gene flow from surface populations. Significantly, phylogeographic studies have provided evidence for speciation and adaptive evolution within the confines of cave environments, questioning the assumption that cave species evolved directly from surface ancestors. Recent technical developments involving 'next generation' DNA sequencing and theoretical developments in coalescent and population modelling are likely to revolutionize the field further, particularly in the study of speciation and the genetic basis of adaptation and convergent evolution within subterranean habitats. In summary, phylogeographic studies have provided an unprecedented insight into the evolution of these unique fauna, and the future of the field should be inspiring and data rich.

VIEWPOINT. Is the Australian subterranean fauna uniquely diverse?

“…These experts used their prior knowledge to assign likely species. (4) Molecular data have proven a major innovation in delineation of new species, both cryptic and otherwise (Juan et al 2010). Hence, in situations in which it was uncertain whether there were distinct species present, genetic methods were used to estimate 'known' but undescribed species from recent collections and molecular studies.…”

“…Colonisation of these habitats by multiple unrelated surface species has also contributed to the high levels of diversity (Leys et al 2003;Cooper et al 2008;Guzik et al 2008). Further, in situ speciation within aquifers is also considered a plausible source of species diversity, particularly in the Yilgarn (Guzik et al 2009;Juan et al 2010) and Pilbara (Finston et al 2009). Abiotic heterogeneity within habitats (i.e.…”

Characteristics of meiofauna in extreme marine ecosystems: a review

“…In some caves of volcanic origin, hydrogen sulphide can reach concentrations of > 300 μM (Riesch et al 2010). These habitats host a unique fauna (Iliffe and Kornicker 2009;Juan et al 2010) and because they represent independent evolutionary trajectories of adaptations to similar conditions, similar to islands for the terrestrial environment, they are considered one of the most important habitats to study marine island biogeography (Dawson 2016).…”

Aphaenogaster gamagumayaa sp. nov.: the first troglobiotic ant from Japan (Hymenoptera: Formicidae: Myrmicinae)

“…It also has reduced eyes, and a less pigmented body than other Aphaenogaster species. Loss of wings, reduction of eyes, elongation of antennae and legs, and loss of pigmentation are commonly observed in troglobiotic arthropods (Vandel 1964, Christiansen 1965, Culver 1982, Marques & Gnaspini 2001Juan et al 2010). It is unclear whether A. gamagumayaa displays any wing loss/reduction in the queen and male, as during the course of the study only workers were found.…”