Distinguishing the effects of selection from demographic history in the genetic variation of two sister passerines based on mitochondrial–nuclear comparison

Abstract

Determining the mechanisms responsible for the distribution of genetic diversity in natural populations has occupied a central role in molecular evolution. Our study was motivated by the unprecedented observation that a widespread Eurasian flycatcher, Ficedula albicilla, exhibited no variation at the mitochondrial DNA (mtDNA) ND2 gene in 75 individuals sampled over a 5000-km distance. In contrast, its sister species, F. parva, had low but considerably higher levels of mtDNA variation. We assessed whether natural selection or demographic factors could explain the absence of mtDNA variation in F. albicilla. Eighteen nuclear genes were sequenced to estimate the two species' phylogeographic histories, and for comparison to the mtDNA data. Multilocus coalescence analyses suggested that F. albicilla experienced a population expansion perhaps following a population bottleneck. Simulations based on this demographic history, however, did not replicate the extremely low level of mtDNA variation. Historical range changes based on ecological niche models also failed to explain the observed mtDNA patterns. Neutrality tests (DHEW and ML-HKA) suggested a non-neutral pattern in the mtDNA of F. albicilla. We found a transmembrane-skewed distribution of nonsynonymous substitutions between the two species, three of which caused functional change; the results implied that positive selection could have targeted mtDNA. Several lines of evidence support selection rather than demographic history as the main force influencing the patterns of mtDNA variation. Despite the influence of natural selection, many of the phylogeographic inferences derived from mtDNA were robust, including species limits and a high level of gene flow among populations within species.

Matching loci surveyed to questions asked in phylogeography

“…By contrast, intra-population genetic diversity can also be strongly influenced by natural selection and changes in population size [11,48,49]. The neutrality tests reveal no evidence of selection on the mtDNA and nuDNA in this study.…”

“…However, our goal here is to provide a retrospective analysis on the mtDNA era of phylogeography and estimate the credibility of nearly three decades of mtDNA studies. Many studies have found that the results based on multiple nuclear genes or genome-wide data are often consistent with those based on one single mtDNA gene data in phylogeographic patterns or species delimitation ( [8,11,[44][45][46]56]; but see [5,41,42]). Here, we provide empirical data confirming the assertion that mtDNA is a useful marker for detecting recent population differentiation because of its fast coalescent time at least in avian taxa (figure 3).…”

“…Homozygous genotypes and genotypes with single heterozygous sites or with indels were included in the PHASE analyses to improve their performance [8]. We tested intra-locus recombination based on recombination rates estimated using a Bayesian method implemented in PHASE [8,11] (see the electronic supplementary material, supplementary methods section, for details).…”

“…It has been suggested that mtDNA data are efficient, considering both experimental cost and accuracy, in detecting phylogeographic patterns [2,7], but might be unreliable for quantifying evolutionary processes [6,8]. In general, genetic divergence between populations is less affected by population size change and selection than genetic diversity within populations [9][10][11]. If so, mtDNA divergence between populations should be a good predictor of actual divergence time.…”

Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

“…Such protein‐altering replacements at positions that are otherwise conserved over large evolutionary timescales may be slightly deleterious or/and counteracted by compensatory changes in the nuclear‐coded mitochondrial proteins (Osada & Akashi ) or may truly reflect adaptation (Veilleux et al . ; Hung & Zink ).…”