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DNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA.

ABSTRACT: Selection is expected to be more efficient in species that are more diverse because both the efficiency of natural selection and DNA sequence diversity are expected to depend upon the effective population size. We explore this relationship across a data set of 751 mammal species for which we have mitochondrial polymorphism data. We introduce a method by which we can examine the relationship between our measure of the efficiency of natural selection, the nonsynonymous relative to the synonymous nucleotide site diversity (?N/?S), and synonymous nucleotide diversity (?S), avoiding the statistical non-independence between the two quantities. We show that these two variables are strongly negatively and linearly correlated on a log scale. The slope is such that as ?S doubles, ?N/?S is reduced by 34%. We show that the slope of this relationship differs between the two phylogenetic groups for which we have the most data, rodents and bats, and that it also differs between species with high and low body mass, and between those with high and low mass-specific metabolic rate.

SUBMITTER: James J

PROVIDER: S-EPMC5176113 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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DNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA.

James J J Castellano D D Eyre-Walker A A

Heredity 20161109 1

Selection is expected to be more efficient in species that are more diverse because both the efficiency of natural selection and DNA sequence diversity are expected to depend upon the effective population size. We explore this relationship across a data set of 751 mammal species for which we have mitochondrial polymorphism data. We introduce a method by which we can examine the relationship between our measure of the efficiency of natural selection, the nonsynonymous relative to the synonymous n ...[more]

PMID: 27827387

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Project description:I examined mitochondrial ND2 sequences in species of tits (genus Parus) to determine whether substitutions were neutral or under selection. Haplotype trees in these species are shallow and geographically unstructured, which could be a signature of recent demographic expansion or purifying selection. McDonald-Kreitman tests revealed a pattern of excess replacement polymorphisms for closely related taxa. Replacement substitutions tended to be less common in the basal parts of haplotype trees, suggesting that they are selected against over evolutionary time. Thus, the pattern of selection is consistent with a model of mildly deleterious haplotypes. To investigate the significance of this selection, the ND2 gene was subdivided into surface and transmembrane portions, and synonymous-non-synonymous sites, and F(ST)-values (the amount of variance distributed among populations) computed for each. Among sampling localities in P. major, both partitions gave similar estimates of F(ST), which is consistent with demographic expansion as the cause of the shallow trees. In P. montanus, two localities contained high percentages of individuals that had a single replacement substitution in the transmembrane portion of the gene, which inflated F(ST)-values relative to the surface sites. Thus, the interpretation of the genetic differentiation of these two sites could be either geographical isolation or selection. Given that the sole substitution causing the high F(ST)-values was a replacement one, selection is implicated. However, this substitution occurred in only 2 of 12 localities, revealing that overall the phylogeographic pattern was not biased by selection, once the cause of the two high pairwise F(ST)-comparisons was recognized. Investigators should consider the source of significant genetic heterogeneity within species, to determine if the variation is likely caused by demographic isolation or selection. However, it seems unlikely that most phylogeographic analyses are invalidated by the effects of natural selection.

Project description:The trajectories of postglacial range expansions, the occurrence of lineage patches and the formation and maintenance of secondary contact between lineages may mostly reflect neutral demographic processes, including density blocking, that may leave long-lasting genetic signatures. However, a few studies have recently shown that climate may also play a role. We used red deer, a large, mobile herbivore that is assumed to be sensitive to climate change, to test hypotheses of possible selection on the mitochondrial DNA cytochrome b gene (mtDNA cytb) and competitive and/or density-blocking (using mtDNA control region). We searched for a possible link between the phylogeographic structure and abiotic climatic variables. Finally, we tested for isolation by distance and isolation by environment and assessed the impact of human-mediated translocations on the genetic structure of red deer. Our analysis of 30 red deer populations in Poland using the mtDNA control region (N = 357) and cytochrome b (N = 50) markers not only confirmed the presence of the Western and South-Eastern lineages of the species but also indicated the presence of a previously unnoticed, rare relic haplotype that grouped together C. e. italicus from Italy (the Mesola deer). No significant signs of positive selection were detected for the mtDNA cytb gene in the studied red deer. However, a significant signal for purifying selection was found in our study that may explain the narrowness of the contact zone because gene flow between the Western and South-Eastern lineages should drive relatively strong mito-nuclear incompatibilities. MtDNA control region differentiation among red deer populations in Poland correlated with different abiotic climatic variables. Strikingly, the southernmost ice sheet limits during the Elsterian was the most important factor, and it explained the largest amount of variation. However, neither isolation by distance (IBD) nor isolation by environment (IBE) were recorded, and a very limited impact of human translocations was evident. The above-mentioned results suggest that in contemporary red deer populations in Poland, the phylogeographic pattern is well preserved, and long-term processes (density and/or competitive blocking) still play a major role.

Dataset Information

DNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA.

Publications

DNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA.

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