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Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles.

ABSTRACT: Regressive evolution, the reduction or total loss of non-functional characters, is a fairly common evolutionary phenomenon in subterranean taxa. However, the genetic basis of regressive evolution is not well understood. Here we investigate the molecular evolution of the eye pigment gene cinnabar in several independently evolved lineages of subterranean water beetles using maximum likelihood analyses. We found that in eyeless lineages cinnabar has an increased rate of sequence evolution, as well as mutations leading to frame shifts and stop codons, indicative of pseudogenes. These results are consistent with the hypothesis that regressive evolution of eyes proceeds by random mutations, in the absence of selection, that ultimately lead to the loss of gene function in protein-coding genes specific to the eye pathway.

SUBMITTER: Leys R

PROVIDER: S-EPMC1626372 | biostudies-literature | 2005 Dec

REPOSITORIES: biostudies-literature

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Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles.

Leys Remko R Cooper Steven J B SJ Strecker Ulrike U Wilkens Horst H

Biology letters 20051201 4

Regressive evolution, the reduction or total loss of non-functional characters, is a fairly common evolutionary phenomenon in subterranean taxa. However, the genetic basis of regressive evolution is not well understood. Here we investigate the molecular evolution of the eye pigment gene cinnabar in several independently evolved lineages of subterranean water beetles using maximum likelihood analyses. We found that in eyeless lineages cinnabar has an increased rate of sequence evolution, as well ...[more]

PMID: 17148242

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Project description:BackgroundSpecies thermal requirements are one of the principal determinants of their ecology and biogeography, although our understanding of the interplay between these factors is limited by the paucity of integrative empirical studies. Here we use empirically collected thermal tolerance data in combination with molecular phylogenetics/phylogeography and ecological niche modelling to study the evolution of a clade of three western Mediterranean diving beetles, the Agabus brunneus complex.ResultsThe preferred mitochondrial DNA topology recovered A. ramblae (North Africa, east Iberia and Balearic islands) as paraphyletic, with A. brunneus (widespread in the southwestern Mediterranean) and A. rufulus (Corsica and Sardinia) nested within it, with an estimated origin between 0.60-0.25 Ma. All three species were, however, recovered as monophyletic using nuclear DNA markers. A Bayesian skyline plot suggested demographic expansion in the clade at the onset of the last glacial cycle. The species thermal tolerances differ significantly, with A. brunneus able to tolerate lower temperatures than the other taxa. The climatic niche of the three species also differs, with A. ramblae occupying more arid and seasonal areas, with a higher minimum temperature in the coldest month. The estimated potential distribution for both A. brunneus and A. ramblae was most restricted in the last interglacial, becoming increasingly wider through the last glacial and the Holocene.ConclusionsThe A. brunneus complex diversified in the late Pleistocene, most likely in south Iberia after colonization from Morocco. Insular forms did not differentiate substantially in morphology or ecology, but A. brunneus evolved a wider tolerance to cold, which appeared to have facilitated its geographic expansion. Both A. brunneus and A. ramblae expanded their ranges during the last glacial, although they have not occupied areas beyond their LGM potential distribution except for isolated populations of A. brunneus in France and England. On the islands and possibly Tunisia secondary contact between A. brunneus and A. ramblae or A. rufulus has resulted in introgression. Our work highlights the complex dynamics of speciation and range expansions within southern areas during the last glacial cycle, and points to the often neglected role of North Africa as a source of European biodiversity.

Project description:BACKGROUND:Cave 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. RESULTS:Ca. 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. CONCLUSIONS:Our 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.

Dataset Information

Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles.

Publications

Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles.

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