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Strong selective effects of mitochondrial DNA on the nuclear genome

TitleStrong selective effects of mitochondrial DNA on the nuclear genome
Publication TypeJournal Article
Year of Publication2020
AuthorsHealy T.M, Burton RS
Volume117
Pagination6616-6621
Date Published2020/03
Type of ArticleArticle
ISBN Number0027-8424
Accession NumberWOS:000521821800048
KeywordsBioenergetics; breakdown; coevolution; copepod; copepod tigriopus-californicus; cytochrome-c genotypes; differentiation; evolution; hybrid; incompatibilities; intergenomic; mitonuclear; populations; replacement; Science & Technology - Other Topics
Abstract

Oxidative phosphorylation, the primary source of cellular energy in eukaryotes, requires gene products encoded in both the nuclear and mitochondrial genomes. As a result, functional integration between the genomes is essential for efficient adenosine triphosphate (ATP) generation. Although within populations this integration is presumably maintained by coevolution, the importance of mitonuclear coevolution in key biological processes such as speciation and mitochondrial disease has been questioned. In this study, we crossed populations of the intertidal copepod Tigriopus californicus to disrupt putatively coevolved mitonuclear genotypes in reciprocal F-2 hybrids. We utilized interindividual variation in developmental rate among these hybrids as a proxy for fitness to assess the strength of selection imposed on the nuclear genome by alternate mitochondrial genotypes. Developmental rate varied among hybrid individuals, and in vitro ATP synthesis rates of mitochondria isolated from high-fitness hybrids were approximately two-fold greater than those of mitochondria isolated from low-fitness individuals. We then used Pool-seq to compare nuclear allele frequencies for high- or low-fitness hybrids. Significant biases for maternal alleles were detected on 5 (of 12) chromosomes in high-fitness individuals of both reciprocal crosses, whereas maternal biases were largely absent in low-fitness individuals. Therefore, the most fit hybrids were those with nuclear alleles that matched their mitochondrial genotype on these chromosomes, suggesting that mitonuclear effects underlie individual-level variation in developmental rate and that intergenomic compatibility is critical for high fitness. We conclude that mitonuclear interactions can have profound impacts on both physiological performance and the evolutionary trajectory of the nuclear genome.

DOI10.1073/pnas.1910141117
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