Gene flow prevents mitonuclear co-adaptation: A comparative portrait of sympatric wild types and cybrids in the fish Chrosomus eos.

Allospecific mtDNA can occasionally be beneficial for the fitness of populations. It is, however, difficult to assess the effect of mtDNA in natural conditions due to genetic and/or environmental interactions. In the fish Chrosomus eos, the transfer of C. neogaeus mitochondria occurs in a single generation and results in natural cybrids. For a few lakes in Quebec, C. eos can harbor either a C. eos mtDNA (wild types) or a C. neogaeus mtDNA (cybrids). Moreover, mtDNA of cybrids originated either from Mississippian or Atlantic glacial refuges. Such diversity provides a useful system for in situ assessment of allospecific mtDNA effects. We determined genetic, epigenetic and transcriptomic variation as well as mitochondrial enzymatic activity (complex IV) changes among wild types and cybrids either in sympatry or allopatry. Wild types and cybrids did not segregate spatially within a lake. Moreover, no significant genetic differentiation was detected among wild types and cybrids indicating sustained gene flow. Mitochondrial complex IV activity was higher for cybrids in both sympatry and allopatry while no difference was detected among cybrid haplotypes. Epigenetic and transcriptomic analyses revealed only subtle differences between sympatric wild types and cybrids compared to differences between sites. Altogether, these results indicate a limited influence of allospecific mtDNA in nuclear gene expression when controlling for genetic and environmental effects. The absence of a reproductive barrier between wild types and cybrids results in random association of either C. eos or C. neogaeus mtDNA with C. eos nDNA at each generation, and prevents mitonuclear co-adaptation in sympatry.

The effects of allospecific mitochondrial genome on the fitness of northern redbelly dace (Chrosomus eos).

Instantaneous mitochondrial introgression events allow the disentangling of the effects of hybridization from those of allospecific mtDNA. Such process frequently occurred in the fish Chrosomus eos, resulting in cybrid individuals composed of a C. eos nuclear genome but with a C. neogaeus mtDNA. This provides a valuable model to address the fundamental question: How well do introgressed individuals perform in their native environment? We infer where de novo production of cybrids occurred to discriminate native environments from those colonized by cybrids in 25 sites from two regions (West-Qc and East-Qc) in Quebec (Canada). We then compared the relative abundance of wild types and cybrids as a measure integrating both fitness and de novo production of cybrids. According to mtDNA variation, 12 introgression events are required to explain the diversity of cybrids. Five cybrid lineages could not be associated with in situ introgression events. This includes one haplotype carried by 93% of the cybrids expected to have colonized West-Qc. These cybrids also displayed a nearly complete allopatric distribution with wild types. We still inferred de novo production of cybrids at seven sites, that accounted for 70% of the cybrids in East-Qc. Wild-type and cybrid individuals coexist in all East-Qc sites while cybrids were less abundant. Allopatry of cybrids restricted to the postglacial expansion suggests the existence of higher fitness for cybrids in specific conditions, allowing for the colonization of different environments and expanding the species' range. However, allospecific mtDNA does not provide a higher fitness to cybrids in their native environment compared to wild types, making the success of an introgressed lineage uncertain.

Interactions between nuclear genes and a foreign mitochondrial genome in the redbelly dace Chrosomus eos.

Given the coevolution process occurring between nuclear and mitochondrial genomes, the effects of introgressive hybridization remain puzzling. In this study, we take advantage of the natural co-occurrence of two biotypes bearing a similar nuclear genome (Chrosomus eos) but harbouring mitochondria from different species (wild type: C. eos; cybrids: Chrosomus neogaeus) to determine the extent of phenotype changes linked to divergence in the mitochondrial genome. Changes were assessed through differences in gene expression, enzymatic activity, proteomic and swimming activity. Our data demonstrate that complex IV activity was significantly higher in cybrids compared to wild type. This difference could result from one variable amino acid on the COX3 mitochondrial subunit and/or from a tremendous change in the proteome. We also show that cybrids present a higher swimming performance than wild type. Ultimately, our results demonstrate that the absence of coevolution for a period of almost ten million years between nuclear and mitochondrial genomes does not appear to be necessarily deleterious but could even have beneficial effects. Indeed, the capture of foreign mitochondria could be an efficient way to circumvent the selection process of genomic coevolution, allowing the rapid accumulation of new mutations in C. eos cybrids.