Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs

Abstract

Interspecies transfer of mitochondrial (mt) DNA is a common phenomenon in plants, invertebrates and vertebrates, normally linked with hybridization of closely related species in zones of sympatry or parapatry. In central Europe, in an area north of 48 degrees N latitude and between 8 degrees and 22 degrees E longitude, western Palaearctic water frogs show massive unidirectional introgression of mtDNA: 33.7% of 407 Rana ridibunda possessed mtDNA specific for Rana lessonae. By contrast, no R. lessonae with R. ridibunda mtDNA was observed. That R. ridibunda with introgressed mitochondrial genomes were found exclusively within the range of the hybrid Rana esculenta and that most hybrids had lessonae mtDNA (90.4% of 335 individuals investigated) is evidence that R. esculenta serves as a vehicle for transfer of lessonae mtDNA into R. ridibunda. Such introgression has occurred several times independently. The abundance and wide distribution of individuals with introgressed mitochondrial genomes show that R. lessonae mt genomes work successfully in a R. ridibunda chromosomal background despite their high sequence divergence from R. ridibunda mtDNAs (14.2-15.2% in the ND2/ND3 genes). Greater effectiveness of enzymes encoded by R. lessonae mtDNA may be advantageous to individuals of R. ridibunda and probably R. esculenta in the northern parts of their ranges.

Fig. 1

Phylogenetic relationships of R. lessonae and R. ridibunda haplotypes. (A) Complete MrBayes maximum posterior tree of all haplotypes with R. shqiperica included as the sister taxon of R. lessonae and two presumptive outgroups of R. ridibunda (R. cretensis and R. epeirotica). (B) R. ridibunda clade: labels mark the ridibunda haplotype (R1–R19) and corresponding sequence numbers (Table 2); (C) R. lessonae clade: labels mark the lessonae haplotype (L1–L17) and sequence number (Table 3). The values at the branches are posterior probabilities for the clade to the right of that branch. The units of the scale bar in A, B and C are the expected mutations per site; B and C are on the same scale. Sequence numbers are specified in Supplementary Material online.

Fig. 2

Geographical distribution of haplotypes found in R. ridibunda and R. esculenta.