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

Abstract

Mitochondrial DNA (mtDNA) is typically passed on to progeny only by the female parent. The phenomenon of "doubly uniparental inheritance" (DUI) of mtDNA in many bivalve species is a fascinating exception to the paradigm of strict maternal inheritance of mtDNA. In this review, we survey the current state of knowledge of DUI, and discuss several active areas of research in this field. Topics/questions covered include: the number of times DUI evolved (once or multiple origins), the link between DUI and sex determination, the role(s) of mtDNA-encoded non-oxidative phosphorylation genes (i.e., ORFan/orf genes) in freshwater mussels, the function of conserved sequence motifs and sperm transmission elements in mtDNA of marine mussels, the challenges of annotating mtDNA genomes of DUI species, the presence of unorthodox features in venerid mtDNA, whether or not orf DNA sequences are useful in species-level identification of freshwater mussel, and finally, whether or not there are obvious benefits of DUI. For each topic we also highlight important avenues for future research within this fascinating field of mitochondrial evolutionary biology.

Relaxed selection on male mitochondrial genes in DUI bivalves eases the need for mitonuclear coevolution

“…Some hypotheses suggest positive selection for enhanced sperm function in male DUI species (Breton et al, 2007;Burt & Trivers, 2006;Skibinski et al, 1994). DUI species can also theoretically escape the "mother's curse" inherent to SMI (Bettinazzi et al, 2019(Bettinazzi et al, , 2020Cosmides & Tooby, 1981;Frank & Hurst, 1996;Gemmell et al, 2004;Stewart et al, 2020), allowing mt variants with adaptive male-specific functions to be selected for. However, experiments using "masculinized" mt genomes in Mytilus edulis do not support this (Everett et al, 2004;Jha et al, 2008).…”

Expanding the Search for Sperm Transmission Elements in the Mitochondrial Genomes of Bivalve Mollusks

“…While this is still the most parsimonious explanation, it is possible that the M-type sequestration mechanism evolved independently three or more times in the history of the Bivalvia. Analysis of additional complete sequences of M and F mitochondrial genomes in the future should help test hypotheses of putative cases of recombination and masculinization within particular bivalve orders, which should, in turn, shed more light on the roles of STEs and uncharacterized mitochondrial open reading frames (ORFs) in the origin and maintenance of DUI across the Bivalvia [8].…”

“…A diagram reiterating the homology between the definitive STE motif to other known STE signatures within closely related mytilids, as was originally proposed by Kyriakou et al [10], is given in Figure 1a. As discussed elsewhere [8], the extremely short nucleotide length of the STE motif causes a significant challenge for identifying homologous STE signatures across Bivalvia. As an extreme example, the similarity between a previously described M. trossulus male-type STE versus the functional/known M. galloprovincialis RM-type STE was reported as~63% (Figure 1a; also see [10] and the figures given therein).…”

“…In addition to marine mussels, DUI has been found in marine clams of the order Veneroida, freshwater mussels of the order Unionoida, and nutshells of the order Nuculanoida; however, the phylogenetic position of Nuculanoida (e.g., Yoldia) within or outside of the Protobranchia is controversial [1,7]. In a recent review of current research in the area of DUI, Stewart and colleagues [8] discussed the following topics: whether DUI evolved once or multiple origins, the challenges of annotating mtDNA genomes of DUI species, whether there is a link between the male-and female-transmitted mtDNA genomes and sex determination, what possible role(s) non-oxidative phosphorylation mitochondrial genes (i.e., open reading frames or ORFs) may play in freshwater mussels, and whether or not there are obvious evolutionary advantages of DUI, among other questions. One of the other points of discussion briefly considered was the possible function of conserved sequence motifs and sperm transmission elements (STEs) in the mitochondrial genomes of marine mussels.…”

The complete mitogenome of the inarticulate brachiopod Glottidia pyramidata reveals insights into gene order variation, deviant ATP8 and mtORFans in the Brachiopoda

“…Interestingly, some of the few brachiopod mitochondrial DNAs (mtDNAs) sequenced to date resemble those of bivalves with DUI (i.e. with doubly uniparental inheritance of mtDNA characterized by the presence of two sex-associated mtDNA lineages inherited through males and females, respectively; Breton et al 2007 ; Stewart et al 2020 ). As for DUI bivalves (e.g.…”