Footprints of unconventional mitochondrial inheritance in bivalve phylogeny: Signatures of positive selection on clades with doubly uniparental inheritance

Abstract

The doubly uniparental inheritance (DUI) of some bivalve mollusks is the major exception to the common maternal inheritance of mitochondria in animals. DUI involves two mitochondrial lineages with paternal and maternal transmission routes, and it appears as a complex phenomenon requiring both nuclear and mitochondrial adaptations. DUI distribution seems to be scattered among the Bivalvia, and there are several clues for its multiple origins. In this paper, we investigate whether the incipient DUI systems had left possible selective signatures on mitochondrial genomes. Alongside the outstanding divergence of amino acid sequences, we confirmed strong purifying selection to act on mitochondrial genes. However, we found evidence that distinct episodes of intense directional pressure are associated with the origins of different DUI systems: We interpret these signals as footprints of the coevolution with the nuclear genome that ought to take place at the base of a DUI clade. Six genes (atp6, cox1, cox2, cox3, nad4L, and nad6) seem to be more commonly linked to the appearance of DUI. We also identified few putative DUI‐specific mutations, thus extending support to the hypothesis of multiple independent origins of this complex phenomenon.

Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

“…2a,c). These results are consistent with the general findings in DUI bivalves 32 . For S. plana the average nucleotide divergence (measured as p-distance) of combined protein coding and ribosomal RNA genes is 0.43 ± 0.08 SD (based on values in Fig.…”

“…Overall, our results are in line with what has been observed in other bivalves with DUI, i.e. despite the considerable divergence of DNA and amino acid sequences of PCGs there is evidence of strong purifying selection acting on these mitochondrial genes 32 . For comparative purpose, p-distances of individual genes (PCGs only) between F and M mtDNAs were also calculated for three species known for having the greatest F versus M DNA divergences in the families Mytilidae, Veneridae and Unionidae: i.e., the mytilid Modiolus modiolus 53 , the venerid Ruditapes philippinarum 17 , and the unionid Quadrula quadrula 14 (Table 4).…”

An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

“…A central tenant of DUI is that the heteroplasmy observed in bivalves is sex-linked (Ghiselli et al 2019). However, for such a pattern to occur, it logically must follow that genetic mechanism(s) exist to facilitate the cellular recognition of male versus female mitochondria/mitotypes (see Plazzi and Passamonti [2019], and particularly Zouros [2020], for more advanced discussions on genetic signatures/models of DUI). Recent work on the description of sperm transmission elements (STEs) and DUI-associated orf genes has attempted to identify major regions presumed to convey female or male genetic signature(s).…”

Linking paternally inherited mtDNA variants and sperm performance

“…To date, DUI has been detected in more than 100 bivalve species and its distribution appears to be scattered [28]. Although a single origin of DUI near the origin of the modern class Bivalvia would represent the most parsimonious hypothesis, there is evidence for multiple independent origins of this peculiar system [24,28,29]. This is reflected at the phylogenetic level, where F-and M-mitotypes of different species sometimes join according to their gender linkage, as seen in freshwater mussels, or they cluster together according to species relatedness, as seen in several marine species [28][29][30][31].…”