Extensive Introgression of Mitochondrial Dna Relative to Nuclear Genes in the Drosophila Yakuba Species Group

Abstract

Abstract. Studies of gene flow between recently diverged species can illuminate the role of natural selection in the formation of new species. Drosophila santomea and D. yakuba are recently diverged, partially reproductively isolated species that continue to hybridize in the wild, and appear to be reproductively isolated from the more distantly related species D. teissieri. We examine patterns of nucleotide polymorphism and divergence in these three species at multiple X-linked, Y-linked, and mitochondrial markers. All three species harbor drastically reduced variability on the Y chromosome relative to the X, as expected for a nonrecombining chromosome subject to variation-reducing selection. The three species are generally well differentiated at the nuclear markers, with little evidence for recent introgression for either the X-or Y-linked genes. Based on the nuclear genes, we estimate that D. santomea and D. yakuba diverged about one-half million years ago and split from D. teissieri about one million years ago. In contrast to the pattern at nuclear loci, all three species share a very similar mtDNA haplotype. We show that the mtDNA must have recently introgressed across species boundaries in the D. yakuba subgroup and that its fixation was driven by either selection on the mitochondria itself or other cytoplasmic factors. These results demonstrate that different regions of the genome can have distinct evolutionary dynamics in the context of species formation. Although natural selection is usually thought of as accentuating divergence between species, our results imply that it can also act as a homogenizing force.

Selection, Recombination and Demographic History in Drosophila miranda

“…Emerging evidence for complicated demographies in many Drosophila species (Machado et al 2002;Wall et al 2002;Haddrill et al 2005b;Kopp and Barmina 2005;Bachtrog et al 2006;Baudry et al 2006) suggests that using comparative approaches to address the question of how common adaptive evolution is may need to involve comparisons of many species. In addition to nonequilibrium demography, nonequilibrium mutation models might also result in discrepancies in estimates of a among species (Eyre-Walker 1997; Kern and Begun 2005;Akashi et al 2006), although their quantitative effects on estimates of adaptive evolution have yet been little investigated.…”

“…In addition, large data sets in D. melanogaster suggest far more than expected heterogeneity in relative levels of polymorphism and divergence across the genome both in recently founded (Glinka et al 2003;Orengo and Aguade 2004) and in older (Haddrill et al 2005b) populations. While these patterns have been interpreted in the context of selection models Begun and Whitley 2000;Andolfatto 2001;Orengo and Aguade 2004;Ometto et al 2005), purely demographic hypotheses have proven difficult to reject as alternative explanations (Wall et al 2002;Haddrill et al 2005b;Thornton and Andolfatto 2006). One approach to making further progress in distinguishing demographic and selective effects on genome variability is either to focus on populations that are likely to have had a more stable demographic history (e.g., Andolfatto and Wall 2003) or to use a comparative approach by investigating genomewide variability patterns in more species.…”

The biogeography of mitochondrial and nuclear discordance in animals

“…In these cases, significantly less mtDNA divergence compared with nuclear differentiation can implicate mitochondrial introgression between taxa (e.g. Cathey et al 1998;Bachtrog et al 2006;Irwin et al 2009). …”

Islands as model systems in ecology and evolution: prospects fifty years after MacArthur‐Wilson

“…Determining the genomic signature of speciation with and without gene flow In an insightful paper, Bachtrog et al (2006) proposed that different levels of gene flow during speciation can be distinguished using genealogical analysis of multilocus datasets from closely related species. They argued that under strict allopatry (i.e., no gene flow), all regions of the genome will have a single divergence history, and vary only in their coalescence times (Fig.…”

“…Under these conditions, same-island vs. different-island species pairs offer a promising investigative framework. Coalescent analyses (Sousa & Hey 2013) of multiple species pairs from the same island radiation within such a framework would provide the data to test whether the alternatives proposed by Bachtrog et al (2006) correctly depict genomic patterns of divergence in nature. If the alternatives are supported, such results may offer a baseline to infer levels of gene flow during speciation, in cases where past biogeography (geographic proximity of lineages) is highly uncertain.…”