Ancient origin of a Western Mediterranean radiation of subterranean beetles

Abstract

BackgroundCave organisms have been used as models for evolution and biogeography, as their reduced above-ground dispersal produces phylogenetic patterns of area distribution that largely match the geological history of mountain ranges and cave habitats. Most current hypotheses assume that subterranean lineages arose recently from surface dwelling, dispersive close relatives, but for terrestrial organisms there is scant phylogenetic evidence to support this view. We study here with molecular methods the evolutionary history of a highly diverse assemblage of subterranean beetles in the tribe Leptodirini (Coleoptera, Leiodidae, Cholevinae) in the mountain systems of the Western Mediterranean.ResultsCa. 3.5 KB of sequence information from five mitochondrial and two nuclear gene fragments was obtained for 57 species of Leptodirini and eight outgroups. Phylogenetic analysis was robust to changes in alignment and reconstruction method and revealed strongly supported clades, each of them restricted to a major mountain system in the Iberian peninsula. A molecular clock calibration of the tree using the separation of the Sardinian microplate (at 33 MY) established a rate of 2.0% divergence per MY for five mitochondrial genes (4% for cox1 alone) and dated the nodes separating the main subterranean lineages before the Early Oligocene. The colonisation of the Pyrenean chain, by a lineage not closely related to those found elsewhere in the Iberian peninsula, began soon after the subterranean habitat became available in the Early Oligocene, and progressed from the periphery to the centre.ConclusionsOur results suggest that by the Early-Mid Oligocene the main lineages of Western Mediterranean Leptodirini had developed all modifications to the subterranean life and were already present in the main geographical areas in which they are found today. The origin of the currently recognised genera can be dated to the Late Oligocene-Miocene, and their diversification can thus be traced to Miocene ancestors fully adapted to subterranean life, with no evidence of extinct epigean, less modified lineages. The close correspondence of organismal evolution and geological record confirms them as an important study system for historical biogeography and molecular evolution.

Nucleotide substitution rates for the full set of mitochondrial protein-coding genes in Coleoptera

“…A similar rate was also found in other studies comparing more closely related species of Coleoptera and using different combinations of mitochondrial genes, both ribosomal and protein-coding (e.g., Leys et al, 2003;Pons and Vogler, 2005;Pons et al, 2006;Balke et al, 2009;Ribera et al, 2010).…”

“…In a study with closely related species of Adephaga, Pons et al (2005) found slower rates for cox1 (0.0167 versus 0.0861 subs/s/my/l) but similar rates to those estimated here for cob (0.0211 versus 0.0171 subs/site/my/l, Table 4). Ribera et al (2010) also found slower cox1 rates (0.02 subs/site/my/l) for a group of Polyphagan cave beetles in a time interval of ~40 MY, estimated with a single GTR+I+G model. A similar study performed on complete mitochondrial genomes of 27 salamander species, and using partitioning by codon sites showed a similar trend (Mueller, 2006).…”

Thermal niche evolution and geographical range expansion in a species complex of western Mediterranean diving beetles

“…To establish a temporal framework for the origin and evolution of the A. brunneus complex we used the mitochondrial genes only, for which there are recent calibrations for different families of Coleoptera with very homogeneous estimations for the rate of a combination of protein coding and ribosomal mitochondrial regions, calibrated with fossils and different biogeographic events [39][40][41]. As a prior we used a normal distribution with an average combined rate of 0.01 substitutions/site/million years (MY) and a standard deviation of 0.001, with other settings identical to the above analysis.…”

Phototransduction and clock gene expression in the troglobiont beetlePtomaphagus hirtusof Mammoth cave

“…The major beetle families found in caves are ground beetles (Carabidae: Trechinae), followed by small carrion beetles (Cholevidae or Cholevinae within Leiodidae) and rove beetles (Staphylinidae) (Moldovan, 2005) with large distributions in the palearctic and nearctic ecozones. In addition, a large diversity of aquatic troglobiotic diving beetles (Dytiscidae) has been discovered in Australia (Faille et al, 2010;Leys and Watts, 2008;Leys et al, 2003;Ribera et al, 2010). The Coleoptera are thus an ideal study group to explore the breadth of cave-adaptive states.…”