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

Deremiens, Léo; Schwartz, Logan S.; Angers, Annie; Glémet, Hélène; Angers, Bernard

doi:10.1016/j.cbpb.2015.08.002

Cited by 13 publications

(12 citation statements)

References 58 publications

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“…; Deremiens et al . ). Therefore, the vast majority of cases of purported adaptive mitochondrial introgression are based on indirect evidence or solely on speculation.…”

Section: Mitochondrial Introgressionmentioning

confidence: 99%

The on‐again, off‐again relationship between mitochondrial genomes and species boundaries

2017

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The study of reproductive isolation and species barriers frequently focuses on mitochondrial genomes and has produced two alternative and almost diametrically opposed narratives. On one hand, mtDNA may be at the forefront of speciation events, with co-evolved mitonuclear interactions responsible for some of the earliest genetic incompatibilities arising among isolated populations. On the other hand, there are numerous cases of introgression of mtDNA across species boundaries even when nuclear gene flow is restricted. We argue that these seemingly contradictory patterns can result from a single underlying cause. Specifically, the accumulation of deleterious mutations in mtDNA creates a problem with two alternative evolutionary solutions. In some cases, compensatory or epistatic changes in the nuclear genome may ameliorate the effects of mitochondrial mutations, thereby establishing coadapted mitonuclear genotypes within populations and forming the basis of reproductive incompatibilities between populations. Alternatively, populations with high mitochondrial mutation loads may be rescued by replacement with a more fit, foreign mitochondrial haplotype. Coupled with many nonadaptive mechanisms of introgression that can preferentially affect cytoplasmic genomes, this form of adaptive introgression may contribute to the widespread discordance between mitochondrial and nuclear genealogies. Here, we review recent advances related to mitochondrial introgression and mitonuclear incompatibilities, including the potential for cointrogression of mtDNA and interacting nuclear genes. We also address an emerging controversy over the classic assumption that selection on mitochondrial genomes is inefficient and discuss the mechanisms that lead lineages down alternative evolutionary paths in response to mitochondrial mutation accumulation.

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“…; Deremiens et al . ). Therefore, the vast majority of cases of purported adaptive mitochondrial introgression are based on indirect evidence or solely on speculation.…”

Section: Mitochondrial Introgressionmentioning

confidence: 99%

The on‐again, off‐again relationship between mitochondrial genomes and species boundaries

2017

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“…Nonetheless, the absence of coevolution is not always deleterious. For example, a recent study of the redbelly dace (Chrosomus eos) showed that introgression of a foreign mitogenome, of up to 10 Myr of independent evolution, is not necessarily deleterious but may rather have beneficial effects (Deremiens et al, 2015). In total, few good cases of cytonuclear incompatibility exist outside the laboratory and more empirical evidence is needed to understand the significance of this mechanism in speciation (Burton et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Assessing pre- and post-zygotic barriers between North Atlantic eels (Anguilla anguilla and A. rostrata)

et al. 2016

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Elucidating barriers to gene flow is important for understanding the dynamics of speciation. Here we investigate pre-and post-zygotic mechanisms acting between the two hybridizing species of Atlantic eels: Anguilla anguilla and A. rostrata. Temporally varying hybridization was examined by analyzing 85 species-diagnostic single-nucleotide polymorphisms (SNPs; F ST ⩾ 0.95) in eel larvae sampled in the spawning region in the Sargasso Sea in 2007 (N = 92) and 2014 (N = 460). We further investigated whether genotypes at these SNPs were nonrandomly distributed in post-F1 hybrids, indicating selection. Finally, we sequenced the mitochondrial ATP6 and nuclear ATP5c1 genes in 19 hybrids, identified using SNP and restriction site associated DNA (RAD) sequencing data, to test a previously proposed hypothesis of cytonuclear incompatibility leading to adenosine triphosphate (ATP) synthase dysfunction and selection against hybrids. No F1 hybrids but only later backcrosses were observed in the Sargasso Sea in 2007 and 2014. This suggests that interbreeding between the two species only occurs in some years, possibly controlled by environmental conditions at the spawning grounds, or that interbreeding has diminished through time as a result of a declining number of spawners. Moreover, potential selection was found at the nuclear and the cytonuclear levels. Nonetheless, one glass eel individual showed a mismatch, involving an American ATP6 haplotype and European ATP5c1 alleles. This contradicted the presence of cytonuclear incompatibility but may be explained by that (1) cytonuclear incompatibility is incomplete, (2) selection acts at a later life stage or (3) other genes are important for protein function. In total, the study demonstrates the utility of genomic data when examining pre-and post-zyotic barriers in natural hybrids.

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“…The disruption of this coevolution may impair the catalytic capacity of the electron transport system and ATP synthase enzymes, thus affecting the entire ATP production process and finally the organismal fitness (Barreto & Burton, 2013; Blier, Dufresne, & Burton, 2001). Even if mitonuclear disruption is expected to generally result in negative effects on the phenotype, some positive effects have also been described (Angers, Leung, Vetil, Deremiens, & Vergilino, 2018; Deremiens, Schwartz, Angers, Glemet, & Angers, 2015; Dey, Barrientos, & Moraes, 2000; Toews, Mandic, Richards, & Irwin, 2014). For example, in the yellow‐rumped warbler ( Setophaga spp.)…”

Section: Introductionmentioning

confidence: 99%

“…Within this complex, cybrids from natural populations revealed a higher activity in one enzyme of the OXPHOS system, the cytochrome c oxidase (COX), whereas other OXPHOS enzymes (i.e., complex I, II, and III) did not show significant differences (Angers, Chapdelaine et al, 2018; Deremiens et al, 2015). A single nonsynonymous mutation resulting in a change in amino acid properties differed between the mitochondrial genes encoding COX subunits of C. eos and C. neogaeus (Deremiens et al, 2015). These biotypes with breaks in the continuity of the mitonuclear coevolution represent an opportunity to compare the parallel evolution of the cytoplasmic genome of species and their nuclear interactions.…”

Section: Introductionmentioning

confidence: 99%

Effects of mitonuclear combination and thermal acclimation on the energetic phenotype

et al. 2020

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Activity of the oxidative phosphorylation complexes rely on intimately associated subunits encoded by the mitochondrial and nuclear genomes. Given the key role of this system in adenosine triphosphate production, genes from both genomes must coevolve. A combination of northern redbelly dace (Chrosomus eos) or finescale dace (C. neogaeus) mitochondrial genome with a C. eos nuclear genome allows for a close examination of a naturally occurring disruption of mitonuclear coevolution. We, therefore, investigated the combined effect of mitonuclear genotypes, acclimation, and temperature on the activity of enzymes linked with the energy metabolism in a sympatric population of wild type and cybrid. As expected, the activity of the nuclear‐encoded citrate synthase was only influenced by temperature while the cytochrome c oxidase (composed of nuclear and mitochondrial subunits from wild type and cybrid individuals) responded differently to temperature. This study provides clear evidence of the extent by which mitonuclear coadaptation could influence aerobic metabolism.

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

Cited by 13 publications

References 58 publications

The on‐again, off‐again relationship between mitochondrial genomes and species boundaries

The on‐again, off‐again relationship between mitochondrial genomes and species boundaries

Assessing pre- and post-zygotic barriers between North Atlantic eels (Anguilla anguilla and A. rostrata)

Effects of mitonuclear combination and thermal acclimation on the energetic phenotype

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