Natural selection on mitochondrial DNA inParusand its relevance for phylogeographic studies

Abstract

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. McDonaldKreitman 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.

Robust Estimates of Divergence Times and Selection with a Poisson Random Field Model: A Case Study of Comparative Phylogeographic Data

“…Previous work has found that selection on mtDNA makes it a poor indicator of population size (Bazin et al 2006;Nabholz et al 2009) or species history (Bensch et al 2006) or is uncorrelated with life history traits (Nabholz et al 2008), but other work suggests that selection is not strong enough to bias phylogenetic inference (Zink 2005). Our results that mtDNA was under weak positive selection differ from previous work showing purifying selection reduced mtDNA genetic variability (Bazin et al 2006;Stewart et al 2008), but evidence of positive selection on mtDNA is not a unique finding.…”

Genetic modulation of energy metabolism in birds through mitochondrial function

“…The importance of the genetic match between mitochondrial DNA and nuclear DNA in regulating metabolic rate in hybrid stonechats supplies further evidence that mitochondrial DNA is subjected to selection (e.g. Ballard & Rand 2005;Zink 2005). Our results imply that a coevolutionary response of mitochondrial and nuclear DNA is involved in the selection on mass-specific metabolic rate (see also Blier et al 2001).…”

“…Maternally inherited, mitochondrial DNA has traditionally been used as neutral marker in phylogeographic studies (Zink & Barrowclough 2008), but an increasing number of studies support the idea that climatic conditions can provide a selective ecological gradient that alters mitochondria haplotype, potentially changing mitochondria function and heat production (Matsuura et al 1993;Mishmar et al 2003;Ballard & Whitlock 2004;Ruiz-Pesini et al 2004;Ballard & Rand 2005;Zink 2005; but see Elson et al 2004). Furthermore, Fontanillas et al (2005) showed a relationship between mitochondrial haplotype and maximal non-shivering thermogenesis in white-toothed shrews from a lowland and an upland population, suggesting selection on mitochondria in these two populations.…”

Highly Discordant Nuclear and Mitochondrial DNA Diversities in Atka Mackerel

“…Positive selection can produce similar reductions in diversity and departures from neutrality as a population expansion, and the same star-like haplotype genealogy expected for neutral genes in a growing population can appear as low-frequency haplotypes accumulate around a selected haplotype. While this mode of selection appears to account for patterns of mtDNA variation in some species (e.g., Schizas et al 2001;Ballard and Whitlock 2004;Ballard and Rand 2005;Zink 2005) and has been inferred for some fishes (Á rnason 2004;Grant et al 2006;Vigliola et al 2007), the accrual of slightly deleterious mutations in whole-mitogenomic comparisons of several gadid species indicated a nearly neutral pattern of evolution (Marshall et al 2008).…”