Evolutionary neutrality of mtDNA introgression: evidence from complete mitogenome analysis in roe deer

Abstract

Introgressive hybridization offers a unique platform for studying the molecular basis of natural selection acting on mitogenomes. Most of the mtDNA protein-coding genes are extremely conserved; however, some of the observed variations have potentially adaptive significance. Here, we evaluated whether the evolution of mtDNA in closely related roe deer species affected by widespread mtDNA introgression is neutral or adaptive. We characterized and compared 16 complete mitogenomes of European (Capreolus capreolus) and Siberian (C. pygargus) roe deer, including four of Siberian origin introgressed into European species. The average sequence divergence of species-specific lineages was estimated at 2.8% and varied across gene classes. Only 21 of 315 fixed differences identified in protein-coding genes represented nonsynonymous changes. Only three of them were determined to have arisen in the C. pygargus lineage since the time to the most recent common ancestor (TMRCA) of both Capreolus species, reflecting a decelerated evolutionary ratio. The almost four-fold higher d N /d S ratio described for the European roe deer lineage is constrained by overall purifying selection, especially pronounced in the ND4 and ND5 genes. We suggest that the highly divergent C. capreolus lineage could have maintained a capability for genomic incorporation of the well-preserved and almost ancestral type of mtDNA present in C. pygargus. Our analyses did not indicate any signs of positive selection for Siberian roe deer mtDNA, suggesting that the present widespread introgression is evolutionarily neutral.

Introgression of mtDNA in Urosaurus lizards: historical and ecological processes

“…Mitochondrial genome introgression in particular is commonplace among animals, and sequence variation in mtDNA has largely been treated as neutral in the evolutionary literature (Ballard & Kreitman ; Matosiuk et al . ). However, mitochondrial genetic variation can be critically important to the fitness of individuals (Dowling et al .…”

“…While considerable evolutionary theory is focused on change within or the splitting of genetic lineages, introgression of genes across species boundaries is also an important evolutionary process (Arnold 1992;Rhymer & Simberloff 1996;Mallet 2005;Schwenk et al 2008). Mitochondrial genome introgression in particular is commonplace among animals, and sequence variation in mtDNA has largely been treated as neutral in the evolutionary literature (Ballard & Kreitman 1995;Matosiuk et al 2014). However, mitochondrial genetic variation can be critically important to the fitness of individuals (Dowling et al 2008), cause numerous diseases (Wallace 1999) and lead to differences in energy generation among species (Castoe et al 2008;Shen et al 2010;Pichaud et al 2012).…”

Complete mitochondrial genome sequence of a Hungarian red deer (Cervus elaphus hippelaphus) from high-throughput sequencing data and its phylogenetic position within the family Cervidae

“…The lack of the ''DHU'' arm in tRNA Ser has been reported in other species of Cervidae [8,21,[25][26][27]35]. The non-coding control region contains conserved sequence blocks, and termination-associated sequences; and can be used for fine-scale population studies, since it is amongst the most rapidly evolving segments in the animal mtDNA [17,19,24,28]. The high-throughput approach for sequencing was useful for obtaining the whole mitochondrial genome of red deer, so this method could be used broadly among animal taxa.…”

“…In some cases, the sequences described may have been misidentified. For example in the case of Capreolus species, from which some are described as belonging to Capreolus pygargus [17], but deposited in GenBank as Capreolus capreolus. A second example of possible species assignation error concerns Mazama rufina and Pudu mephistophiles, which share very similar mtDNA genomes (98.6%).…”

Interspecies introgressive hybridization in spiny frogsQuasipaa(Family Dicroglossidae) revealed by analyses on multiple mitochondrial and nuclear genes

“…Since then, introgressive hybridization has been widely detected in amphibians, birds, and mammals (e.g., Dowling et al., 2016; Matosiuk, Sheremetyeva, Sheremetyev, Saveljev, & Borkowska, 2014; Mccracken, Wilson, & Martin, 2013; Sequeira et al., 2011; Marshall et al, 2011). In the initial study of introgressive hybridization, Mecham (1960) used the morphological analysis of the green tree frog Hyla cinerea and the barking tree frog Hyla gratiosa ; the research has revealed the strong signal of introgressive hybridization between the two species.…”