Dataset Information

Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient.

ABSTRACT: In natural populations, allelic diversity of the major histocompatibility complex (MHC) is commonly interpreted as resulting from positive selection in varying spatiotemporal pathogenic landscapes. Composite pathogenic landscape data are, however, rarely available. We studied the spatial distribution of allelic diversity at two MHC class II loci (DQA, DQB) in hares, Lepus capensis, along a steep ecological gradient in North Africa and tested the role of climatic parameters for the spatial distribution of DQA and DQB proteins. Climatic parameters were considered to reflect to some extent pathogenic landscape variation. We investigated historical and contemporary forces that have shaped the variability at both genes, and tested for differential selective pressure across the ecological gradient by comparing allelic variation at MHC and neutral loci. We found positive selection on both MHC loci and significantly decreasing diversity from North to South Tunisia. Our multinomial linear models revealed significant effects of geographical positions that were correlated with mean annual temperature and precipitation on the occurrence of protein variants, but no effects of co-occurring DQA or DQB proteins, respectively. Diversifying selection, recombination, adaptation to local pathogenic landscapes (supposedly reflected by climate parameters) and neutral demographic processes have shaped the observed MHC diversity and differentiation patterns.

SUBMITTER: Awadi A

PROVIDER: S-EPMC6068193 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient.

Awadi Asma A Ben Slimen Hichem H Smith Steve S Knauer Felix F Makni Mohamed M Suchentrunk Franz F

Scientific reports 20180731 1

In natural populations, allelic diversity of the major histocompatibility complex (MHC) is commonly interpreted as resulting from positive selection in varying spatiotemporal pathogenic landscapes. Composite pathogenic landscape data are, however, rarely available. We studied the spatial distribution of allelic diversity at two MHC class II loci (DQA, DQB) in hares, Lepus capensis, along a steep ecological gradient in North Africa and tested the role of climatic parameters for the spatial distri ...[more]

PMID: 30065344

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Project description:Recent studies of selection on mitochondrial (mt) OXPHOS genes suggest adaptation due mainly to environmental variation. In this context, Tunisian hares that display several external phenotypes with phylogenetically rather homogenous gene pool and shallow population structure provide a good precondition to detect positive selection on mt genes related to environmental/climatic variation, specifically ambient temperature and precipitation.We used codon-based methods along with population genetic data to test for positive selection on ATPase synthase 6 (ATP6) and NADH dehydrogenase 2 (ND2) of cape hares (Lepus capensis) collected along a steep ecological gradient in Tunisia. We found significantly higher differentiation at the ATP6 locus across Tunisia, with sub-humid Mediterranean, semi-arid, and arid Sahara climate than for fourteen unlinked supposedly neutrally evolving nuclear microsatellites and mt control region sequences. This suggested positive selection on ATP6 sequences, which was confirmed by several codon-based tests for one sequence site that together with a second site translated into four different amino acids. Positive selection on ND2 sequences was also confirmed by several codon-based tests. The corresponding frequencies of the two most prevalent variants at each locus varied significantly across climate regions, and our logistic general linear models of occurrence of those proteins indicated significant effects of mean annual temperature for ATP6 and mean minimum temperature of the coldest month of the year for ND2, independent of geographical location, annual precipitation, and the respective co-occurring protein at the second locus. Moreover, presence of the ancestral ATP6 protein, as inferred from phylogenetic networks, was positively affected by the simultaneous presence of the derived ND2 protein and vice versa, independent of temperature, precipitation, or geographic location. Finally, we obtained a significant coevolution signal for the ancestral ATP6 and derived ND2 sequences and vice versa.positive selection was strongly suggested by the population genetic approach and the codon-based tests in both mtDNA genes. Moreover, the two most prevalent proteins at the ATP6 locus were distributed at significantly varying frequencies across the study area with a significant effect of mean annual temperature on the occurrence of the ATP6 proteins independent of geographical coordinates and the co-occuring ND2 protein variant. For ND2, occurrence of the two most frequent protein variants was significantly influenced by the mean minimum temperature of the coldest month, independent of the co-occurring ATP6 protein variant and geographical coordinates. This strongly suggests direct involvement of ambient temperature in the adaptation of the studied mtOXPHOS genes.

Project description:BackgroundAnimal mitochondria play a central role in energy production in the cells through the oxidative phosphorylation (OXPHOS) pathway. Recent studies of selection on different mitochondrial OXPHOS genes have revealed the adaptive implications of amino acid changes in these subunits. In hares, climatic variation and/or introgression were suggested to be at the origin of such adaptation. Here we looked for evidence of positive selection in three mitochondrial OXPHOS genes, using tests of selection, protein structure modelling and effects of amino acid substitutions on the protein function and stability. We also used statistical models to test for climate and introgression effects on sites under positive selection.ResultsOur results revealed seven sites under positive selection in ND4 and three sites in Cytb. However, no sites under positive selection were observed in the COX1 gene. All three subunits presented a high number of codons under negative selection. Sites under positive selection were mapped on the tridimensional structure of the predicted models for the respective mitochondrial subunit. Of the ten amino acid replacements inferred to have evolved under positive selection for both subunits, six were located in the transmembrane domain. On the other hand, three codons were identified as sites lining proton translocation channels. Furthermore, four codons were identified as destabilizing with a significant variation of Δ vibrational entropy energy between wild and mutant type. Moreover, our PROVEAN analysis suggested that among all positively selected sites two fixed amino acid replacements altered the protein functioning. Our statistical models indicated significant effects of climate on the presence of ND4 and Cytb protein variants, but no effect by trans-specific mitochondrial DNA introgression, which is not uncommon in a number of hare species.ConclusionsPositive selection was observed in several codons in two OXPHOS genes. We found that substitutions in the positively selected codons have structural and functional impacts on the encoded proteins. Our results are concordantly suggesting that adaptations have strongly affected the evolution of mtDNA of hare species with potential effects on the protein function. Environmental/climatic changes appear to be a major trigger of this adaptation, whereas trans-specific introgressive hybridization seems to play no major role for the occurrence of protein variants.

Project description:In Israel Eruca sativa has a geographically narrow distribution across a steep climatic gradient that ranges from mesic Mediterranean to hot desert environments. These conditions offer an opportunity to study the influence of the environment on intraspecific genetic variation. For this, we combined an analysis of neutral genetic markers with a phenotypic evaluation in common-garden experiments, and environmental characterization of populations that included climatic and edaphic parameters, as well as geographic distribution. A Bayesian clustering of individuals from nine representative populations based on amplified fragment length polymorphism (AFLP) divided the populations into a southern and a northern geographic cluster, with one admixed population at the geographic border between them. Linear mixed models, with cluster added as a grouping factor, revealed no clear effects of environment or geography on genetic distances, but this may be due to a strong association of geography and environment with genetic clusters. However, environmental factors accounted for part of the phenotypic variation observed in the common-garden experiments. In addition, candidate loci for selection were identified by association with environmental parameters and by two outlier methods. One locus, identified by all three methods, also showed an association with trichome density and herbivore damage, in net-house and field experiments, respectively. Accordingly, we propose that because trichomes are directly linked to defense against both herbivores and excess radiation, they could potentially be related to adaptive variation in these populations. These results demonstrate the value of combining environmental and phenotypic data with a detailed genetic survey when studying adaptation in plant populations. This article describes the use of several types of data to estimate the influence of the environment on intraspecific genetic variation in populations originating from a steep climatic gradient. In addition to molecular marker data, we made use of phenotypic evaluation from common garden experiments, and a broad GIS based environmental data with edaphic information gathered in the field. This study, among others, lead to the identification of an outlier locus with an association to trichome formation and herbivore defense, and its ecological adaptive value is discussed.

Dataset Information

Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient.

Publications

Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient.

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