Rampant historical mitochondrial genome introgression between two species of green pond frogs, Pelophylax nigromaculatus and P. plancyi

Abstract

BackgroundMitochondrial introgression may result in the mitochondrial genome of one species being replaced by that of another species without leaving any trace of past hybridization in its nuclear genome. Such introgression can confuse the species genealogy estimates and lead to absurd inferences of species history. We used a phylogenetic approach to explore the potential mitochondrial genome introgression event(s) between two closely related green pond frog species, Pelophylax nigromaculatus and P. plancyi.ResultsDNA sequence data of one mitochondrial and two nuclear genes from an extensive sampling of the two species were collected, and the genealogies of the three genes were constructed and compared. While the two nuclear genes congruently showed mutual reciprocal monophyly of both species, the mitochondrial phylogeny separated a Korean P. nigromaculatus clade, a paraphyletic central China P. plancyi assemblage, and a large well-supported introgression clade. Within the introgression clade, the mitochondrial haplotypes of the two species were mixed together. This reticulated pattern can be most parsimoniously explained by an ancient mitochondrial introgression event from P. plancyi to P. nigromaculatus that occurred at least 1.36 MYA, followed by multiple recent introgression events from P. nigromaculatus back to P. plancyi within the last 0.63 MY. The re-constitution of previously co-adapted genomes in P. plancyi may be responsible for the recent rampant introgression events. The Korean P. nigromaculatus clade likely represents the only surviving "true" mitochondrial lineage of P. nigromaculatus, and the central China P. plancyi assemblage likely represents the "original" P. plancyi mitochondrial lineage. Refugia in the Korean Peninsula and central China may have played a significant role in preserving these ancient lineages.ConclusionsThe majority of individuals in the two species have either introgressed (P. nigromaculatus) or reclaimed (P. plancyi) mitochondrial genomes while no trace of past hybridization in their nuclear genomes was detected. Asymmetrical reproductive ability of hybrids and continuous backcrossing are likely responsible for the observed mitochondrial introgression. This case is unique in that it includes an ancient "forward" introgression and many recent "backward" introgressions, which re-constitutes the original nuclear and mitochondrial genomes of P. plancyi. This hybrid system provides an excellent opportunity to study cyto-nuclear interaction and co-adaptation.

Mitochondrial genome organization and divergence in hybridizing central European waterfrogs of the Pelophylax esculentus complex (Anura, Ranidae)

“…As expected, P. nigromaculatus and P. plancyi formed the sister clade to P. ridibundus and P. lessonae, with substantial divergence (15.8%) between western and eastern Palaearctic representatives of the genus. The low sequence divergence between P. nigromaculatus and P. plancyi (2.1%), suggestive of intraspecific variation, may be the result of mitochondrial transfer between the two taxa, as recently proposed by Liu et al (2010) who postulated both ancient and recent introgression events between these two species.…”

Genetic divergence in tropical anurans: deeper phylogeographic structure in forest specialists and in topographically complex regions

“…However, it is well known that gene flow can extend beyond species boundaries in amphibians, especially among closely-related forms (e.g. Liu et al 2010;Hedrick 2013;Zieliński et al 2013) and might not be accurately described by mitochondrial markers (Irwin 2002;Currat et al 2008). Hence, phylogeographic comparative analyses of units defined by equivalent divergence times, ideally determined from multiple unlinked nuclear loci, will outperform analyses based on species units and ultimately reveal the effects of natural history and ecological variables on population genetic divergence.…”

The biogeography of mitochondrial and nuclear discordance in animals

“…For instance, sex-biased dispersal, mating and offspring production is a common explanation for mito-nuclear discordance, but behavioural and crossing data have only been collected for a handful of systems. For example, in a genetic survey of the dark-spotted frog (Rana nigromaculata), Liu et al (2010) found that many populations are fixed for the eastern golden frog's (R. plancyi) mtDNA. Data combined from the field and laboratory suggest that all F1 males were sterile, but that females were partially fertile, consistent with Haldane's rule and with patterns of mito-nuclear discordance in natural populations (Liu et al 2010).…”

“…For example, in a genetic survey of the dark-spotted frog (Rana nigromaculata), Liu et al (2010) found that many populations are fixed for the eastern golden frog's (R. plancyi) mtDNA. Data combined from the field and laboratory suggest that all F1 males were sterile, but that females were partially fertile, consistent with Haldane's rule and with patterns of mito-nuclear discordance in natural populations (Liu et al 2010). Unfortunately, these data are difficult to collect in many systems, and researchers instead rely on more general patterns.…”