Mitochondria and the Origin of Species: Bridging Genetic and Ecological Perspectives on Speciation Processes

Abstract

Mitochondria have been known to be involved in speciation through the generation of Dobzhansky–Muller incompatibilities, where functionally neutral co-evolution between mitochondrial and nuclear genomes can cause dysfunction when alleles are recombined in hybrids. We propose that adaptive mitochondrial divergence between populations can not only produce intrinsic (Dobzhansky–Muller) incompatibilities, but could also contribute to reproductive isolation through natural and sexual selection against migrants, post-mating prezygotic isolation, as well as by causing extrinsic reductions in hybrid fitness. We describe how these reproductive isolating barriers can potentially arise through adaptive divergence of mitochondrial function in the absence of mito-nuclear coevolution, a departure from more established views. While a role for mitochondria in the speciation process appears promising, we also highlight critical gaps of knowledge: (1) many systems with a potential for mitochondrially-mediated reproductive isolation lack crucial evidence directly linking reproductive isolation and mitochondrial function; (2) it often remains to be seen if mitochondrial barriers are a driver or a consequence of reproductive isolation; (3) the presence of substantial gene flow in the presence of mito-nuclear incompatibilities raises questions whether such incompatibilities are strong enough to drive speciation to completion; and (4) it remains to be tested how mitochondrial effects on reproductive isolation compare when multiple mechanisms of reproductive isolation coincide. We hope this perspective and the proposed research plans help to inform future studies of mitochondrial adaptation in a manner that links genotypic changes to phenotypic adaptations, fitness, and reproductive isolation in natural systems, helping to clarify the importance of mitochondria in the formation and maintenance of biological diversity.

The Mitochondrial Genome–on Selective Constraints and Signatures at the Organism, Cell, and Single Mitochondrion Levels

“…Additionally, population genetics studies from species and different population isolates from the same species in the copepod Tigriopus californicus (Burton et al, 2006;Ellison and Burton, 2006), in reptiles (chameleons) ( Bar-Yaacov et al, 2015) and in birds (sparrows) (Trier et al, 2014), revealed hybrid incompatibility, which constitutes an important step toward speciation. These pieces of evidence provide strong support for the importance of genetic compatibility between the nuclear and mitochondrial genomes, that when interfered with can either lead to diseases (Gershoni et al, 2014) or lead to the creation of reproductive barriers in both invertebrates and in vertebrates (Gershoni et al, 2009;Trier et al, 2014;Telschow et al, 2019;Tobler et al, 2019). The underlying mechanism of mito-nuclear genetic compatibility has previously been thoroughly discussed at the protein-protein, RNA-protein and protein-mtDNA levels at the whole organism level (Bar-Yaacov et al, 2012;Levin et al, 2014;Hill, 2019;Hill et al, 2019).…”

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

“…While the coevolution of mitochondrial and nuclear genomes does occur, the unique biology of mitochondria complicates our view of a species' evolutionary history [32][33][34][35][36][37][38]. In most metazoans, uniparental inheritance, lack of recombination and high mutation rate of mtDNAs make it difficult to separate the effect of genetic drift from natural selection [39].…”

Genetic hitchhiking, mitonuclear coadaptation, and the origins of mt DNA barcode gaps

“…I also consider a potentially pivotal role played by recombination of mitochondrial chromosomes in the generation of mt DNA barcode gaps. I propose that a better understanding of the evolutionary mechanism that generates the genetic structure of mt DNA across eukaryotes is critical not only with regard to assessing the value of DNA barcodes as a tool in taxonomy (Baker, Tavares, & Elbourne, 2009; Rubinoff, Cameron, & Will, 2006) but also for a better understanding of the process of speciation (Hill, 2016; Sunnucks, Morales, Lamb, Pavlova, & Greening, 2017; Tobler, Barts, & Greenway, 2019).…”