Dataset Information

Protein expression parallels thermal tolerance and ecologic changes in the diversification of a diving beetle species complex.

ABSTRACT: Physiological changes associated with evolutionary and ecological processes such as diversification, range expansion or speciation are still incompletely understood, especially for non-model species. Here we study differences in protein expression in response to temperature in a western Mediterranean diving beetle species complex, using two-dimensional differential gel electrophoresis with one Moroccan and one Iberian population each of Agabus ramblae and Agabus brunneus. We identified proteins with significant expression differences after thermal treatments comparing them with a reference EST library generated from one of the species of the complex (A. ramblae). The colonisation during the Middle Pleistocene of the Iberian peninsula by A. ramblae, where maximum temperatures and seasonality are lower than in the ancestral north African range, was associated with changes in the response to 27?°C in proteins related to energy metabolism. The subsequent speciation of A. brunneus from within populations of Iberian A. ramblae was associated with changes in the expression of several stress-related proteins (mostly chaperons) when exposed to 4?°C. These changes are in agreement with the known tolerance to lower temperatures of A. brunneus, which occupies a larger geographical area with a wider range of climatic conditions. In both cases, protein expression changes paralleled the evolution of thermal tolerance and the climatic conditions experienced by the species. However, although the colonisation of the Iberian peninsula did not result in morphological change, the speciation process of A. brunneus within Iberia involved genetic isolation and substantial differences in male genitalia and body size and shape.

SUBMITTER: Hidalgo-Galiana A

PROVIDER: S-EPMC4675881 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Protein expression parallels thermal tolerance and ecologic changes in the diversification of a diving beetle species complex.

Hidalgo-Galiana A A Monge M M Biron D G DG Canals F F Ribera I I Cieslak A A

Heredity 20150902 1

Physiological changes associated with evolutionary and ecological processes such as diversification, range expansion or speciation are still incompletely understood, especially for non-model species. Here we study differences in protein expression in response to temperature in a western Mediterranean diving beetle species complex, using two-dimensional differential gel electrophoresis with one Moroccan and one Iberian population each of Agabus ramblae and Agabus brunneus. We identified proteins ...[more]

PMID: 26328758

Similar Datasets

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:In most lineages, most species have restricted geographic ranges, with only few reaching widespread distributions. How these widespread species reached their current ranges is an intriguing biogeographic and evolutionary question, especially in groups known to be poor dispersers. We reconstructed the biogeographic and temporal origin of the widespread species in a lineage with particularly poor dispersal capabilities, the diving beetle genus Deronectes (Dytiscidae). Most of the ca. 60 described species of Deronectes have narrow ranges in the Mediterranean area, with only four species with widespread European distributions. We sequenced four mitochondrial and two nuclear genes of 297 specimens of 109 different populations covering the entire distribution of the four lineages of Deronectes, including widespread species. Using Bayesian probabilities with an a priori evolutionary rate, we performed (1) a global phylogeny/phylogeography to estimate the relationships of the main lineages within each group and root them, and (2) demographic analyses of the best population coalescent model for each species group, including a reconstruction of the geographical history estimated from the distribution of the sampled localities. We also selected 56 specimens to test for the presence of Wolbachia, a maternally transmitted parasite that can alter the patterns of mtDNA variability. All species of the four studied groups originated in the southern Mediterranean peninsulas and were estimated to be of Pleistocene origin. In three of the four widespread species, the central and northern European populations were nested within those in the northern areas of the Anatolian, Balkan and Iberian peninsulas respectively, suggesting a range expansion at the edge of the southern refugia. In the Mediterranean peninsulas the widespread European species were replaced by vicariant taxa of recent origin. The fourth species (D. moestus) was proven to be a composite of unrecognised lineages with more restricted distributions around the Western and Central Mediterranean. The analysis of Wolbachia showed a high prevalence of infection among Deronectes, especially in the D. aubei group, where all sequenced populations were infected with the only exception of the Cantabrian Mountains, the westernmost area of distribution of the lineage. In this group there was a phylogenetic incongruence between the mitochondrial and the nuclear sequence, although no clear pattern links this discordance to the Wolbachia infection. Our results suggest that, in different glacial cycles, populations that happened to be at the edge of the newly deglaciated areas took advantage of the optimal ecological conditions to expand their ranges to central and northern Europe. Once this favourable ecological window ended populations become isolated, resulting in the presence of closely related but distinct species in the Mediterranean peninsulas.

Project description:In the face of global warming, both the absolute thermal tolerance of an ectotherm, and its ability to shift its tolerance level via acclimation, are thought to be fundamentally important. Understanding the links between tolerance and its plasticity is therefore critical to accurately predict vulnerability to warming. Previous studies in a number of ectotherm taxa suggest trade-offs in the evolution of thermal tolerance and its plasticity, something which does not, however, apply to Deronectes diving beetles, where these traits are instead positively correlated. Here we revisit the relationship between thermal tolerance and plasticity in these beetles, paying attention to a recently discovered morphological adaptation supporting under water respiration - setal tracheal gills. Hollow setae on the elytra interconnect with the beetle's tracheal system, providing a gas exchange surface that allows oxygen to be extracted directly from the water. This enables individuals to stay submerged for longer than their subelytral air stores would allow. We show that hypoxia reduced heat tolerance, especially when individuals were denied access to air, forcing them to rely solely on aquatic gas exchange. Species with higher densities of these gas-exchanging setae exhibited improved cold tolerance, but reduced heat tolerance and lower plasticity of heat tolerance. Differences in setal tracheal gill density across species were also related to habitat use: species with low gill density were found mainly in intermittent, warmer rivers, where underwater gas exchange is more problematic and risks of surfacing may be smaller. Moreover, when controlling for differences in gill density we no longer found a significant relationship between heat tolerance and its plasticity, suggesting that the previously reported positive relationship between these variables may be driven by differences in gill density. Differences in environmental conditions between the preferred habitats could simultaneously select for characteristic differences in both thermal tolerance and gill density. Such simultaneous selection may have resulted in a non-causal association between cold tolerance and gill density. For heat tolerance, the correlations with gill density could reflect a causal relationship. Species relying strongly on diffusive oxygen uptake via setal tracheal gills may have a reduced oxygen supply capacity and may be left with fewer options for matching oxygen uptake to oxygen demand during acclimation, which could explain their reduced heat tolerance and limited plasticity. Our study helps shed light on the mechanisms that underpin thermal tolerance and plasticity in diving air-breathing ectotherms, and explores how differences in thermal tolerance across species are linked to their selected habitat, morphological adaptations and evolutionary history.

Dataset Information

Protein expression parallels thermal tolerance and ecologic changes in the diversification of a diving beetle species complex.

Publications

Protein expression parallels thermal tolerance and ecologic changes in the diversification of a diving beetle species complex.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets