Characterising Mitochondrial Capture in an Iberian Shrew

Abstract

Mitochondrial introgression raises questions of biogeography and of the extent of reproductive isolation and natural selection. Previous phylogenetic work on the Sorex araneus complex revealed apparent mitonuclear discordance in Iberian shrews, indicating past hybridisation of Sorex granarius and the Carlit chromosomal race of S. araneus, enabling introgression of the S. araneus mitochondrial genome into S. granarius. To further study this, we genetically typed 61 Sorex araneus/coronatus/granarius from localities in Portugal, Spain, France, and Andorra at mitochondrial, autosomal, and sex-linked loci and combined our data with the previously published sequences. Our data are consistent with earlier data indicating that S. coronatus and S. granarius are the most closely related of the three species, confirming that S. granarius from the Central System mountain range in Spain captured the mitochondrial genome from a population of S. araneus. This mitochondrial capture event can be explained by invoking a biogeographical scenario whereby S. araneus was in contact with S. granarius during the Younger Dryas in central Iberia, despite the two species currently having disjunct distributions. We discuss whether selection favoured S. granarius with an introgressed mitochondrial genome. Our data also suggest recent hybridisation and introgression between S. coronatus and S. granarius, as well as between S. araneus and S. coronatus.

Keywords: Iberia; Sorex araneus complex; hybridisation; introgression; karyotype; phylogenetics.

Figure 1

Collection localities of 61 Sorex shrews described here, plus 35 described by Yannic et al. [14] (see text). These localities are in southwestern Europe and Poland (inset). The specimens are classified as S. araneus/coronatus/granarius according to their geographic location [14] and/or nuclear DNA sequences (see text). The species distribution ranges shown on the map are derived from [14]. Interesting features of the nuclear (nu)DNA and mitochondrial (mt)DNA sequences are indicated (also see text).

Figure 2

Maximum likelihood phylogenetic tree (A) and minimum spanning network (B) for mitochondrial CytB sequences of members of the S. araneus complex from southwestern Europe and Poland. Only haplotypes are shown, with geographic location and species indicated by symbols. S. alpinus is the outgroup. Asterisks indicate the haplotypes of individuals from geographic regions where two species occur. Their species designation is justified in the text. Bootstrap support over 1000 replicates is indicated on major internal nodes of the tree (only values of 70% or greater). In the network, bars on branches indicate mutational steps.

Figure 3

Maximum likelihood phylogenetic tree for members of the S. araneus complex from southwestern Europe and Poland, based on concatenated nuclear DNA sequences (1967 bp total) derived from ApoB, BRCA1, DBY7, and ZFX1 sequences. Only haplotypes are shown, with geographic location and species indicated by symbols. S. alpinus is the outgroup. Bootstrap support over 1000 replicates is indicated on major internal nodes (only values of 70% or greater).

Figure 4

Maximum likelihood phylogenetic trees for sequences of the autosomal genes ApoB (A) and BRCA1 (B), the Y-linked marker DBY7 (C), and the X-linked gene ZFX1 (D) of members of the S. araneus complex from southwestern Europe and Poland. Only haplotypes are shown, with geographic location and species indicated by symbols. S. alpinus is the outgroup. Asterisks indicate the haplotypes of individuals from geographic regions where two species occur. Their species designation is justified in the text. Bootstrap support over 1000 replicates is indicated on major internal nodes (only values of 50% or greater).