Fine‐scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia

Abstract

Calcrete aquifers in the arid Yilgarn region of central Western Australia are a biodiversity hotspot for stygofauna. A distinct pattern of interspecific size class variation among subterranean dytiscid beetle species has been observed in 29 of these aquifers where either two or three small, medium and/or large sympatric species are found that are in some cases sister species. We used a 3.5 km(2) grid of bores to sample dytiscids on a fine-scale and employed a comparative phylogeographical and population genetic approach to investigate the origins of a sympatric sister species triplet of diving beetles from a single aquifer. Mitochondrial DNA sequence data from the Cytochrome oxidase c subunit I gene revealed that all three species have high levels of haplotype diversity with ancient (approximately 1 million years ago) intra-specific coalescence of haplotypes, but low levels of nucleotide diversity. Population analyses provide evidence for multiple expansion events within each species. There was spatial heterogeneity in the distribution of genetic variation and abundance both within and among the three taxa. Population analyses revealed significant fine-scale differentiation with isolation by distance for Paroster macrosturtensis and P. mesosturtensis, but not the smallest species P. microsturtensis. Haplotype network analyses provided limited or no evidence for past population fragmentation within the large and small species, but substantial historical divergence was observed in P. mesosturtensis that was not spatially structured. A patchy population structure with contemporaneous and historical isolation by distance in the three species is likely to have been a significant isolating and diversifying force, preventing us from ruling out a potential role for allopatric divergence during speciation of this beetle sister triplet.

Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert

“…A repeated pattern of two to three species of stygobiontic diving beetles is consistently observed within isolated aquifers, some of which are clear sympatric sister species (Leys et al, 2003;Watts and Humphreys, 2006;Guzik et al, 2009). To date, this pattern has been observed in 29 calcretes in which each species occupies non-overlapping size classes, ranging from large (B5 mm) to very small (B1 mm) beetles (Watts and Humphreys, 1999, 2003, 2006.…”

“…However, given the extraordinary number of species observed in cave systems (Poulson and Culver, 1969;Humphreys, 2000Humphreys, , 2008Buhay et al, 2007), this transition, from surface to subterranean environments, is unlikely to be the sole source of species diversification in cave animals and it is possible that some species evolved from troglomorphic ancestors fully adapted to life underground (Juan and Emerson, 2010;Ribera et al, 2010). The difficult nature of gaining access to cave habitats makes this latter hypothesis difficult to investigate; however, a number of key studies have examined these questions (Caccone, 1985;Buhay and Crandall, 2005;Guzik et al, 2009). They observe that, internally, cavernicolous habitats maintain complex genetic systems that, undisturbed, are largely stable over time and can maintain significant levels of genetic diversity (Culver, 1970a, b;Culver et al, 1973).…”

“…Currently, it is difficult to test the scenario of sympatric speciation, but identifying whether microallopatric speciation processes, such as population fragmentation, have operated within calcrete aquifers is a distinct possibility. Guzik et al (2009) investigated the population genetic and phylogeographic structure of three sympatric sister species of dytiscid diving beetle from a single aquifer. Their results revealed evidence for isolation by distance (IBD) effects in two of the three beetle species over a very small spatial scale.…”

VIEWPOINT. Is the Australian subterranean fauna uniquely diverse?

“…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.…”

“…In the Yilgarn and Pilbara regions a myriad of short-range endemic species, including both stygobitic (Taiti and Humphreys 2001;Leys et al 2003;Leys and Watts 2008;Page et al 2008;Guzik et al 2009;Bradford et al 2010) and troglobitic (Humphreys and Adams 2001;Harvey et al 2008) taxa have been identified. Much of this diversity is likely to have resulted from vicariance associated with the aridification of the Australian continent after the late Miocene (Byrne et al 2008), which led to biotic isolation of calcretes and other subterranean habitats (e.g.…”