Mitonuclear mismatch alters nuclear gene expression in naturally introgressed Rhinolophus bats

Abstract

Background Mitochondrial function involves the interplay between mitochondrial and nuclear genomes. Such mitonuclear interactions can be disrupted by the introgression of mitochondrial DNA between taxa or divergent populations. Previous studies of several model systems (e.g. Drosophila) indicate that the disruption of mitonuclear interactions, termed mitonuclear mismatch, can alter nuclear gene expression, yet few studies have focused on natural populations. Results Here we study a naturally introgressed population in the secondary contact zone of two subspecies of the intermediate horseshoe bat (Rhinolophus affinis), in which individuals possess either mitonuclear matched or mismatched genotypes. We generated transcriptome data for six tissue types from five mitonuclear matched and five mismatched individuals. Our results revealed strong tissue-specific effects of mitonuclear mismatch on nuclear gene expression with the largest effect seen in pectoral muscle. Moreover, consistent with the hypothesis that genes associated with the response to oxidative stress may be upregulated in mitonuclear mismatched individuals, we identified several such gene candidates, including DNASE1L3, GPx3 and HSPB6 in muscle, and ISG15 and IFI6 in heart. Conclusion Our study reveals how mitonuclear mismatch arising from introgression in natural populations is likely to have fitness consequences. Underlying the processes that maintain mitonuclear discordance is a step forward to understand the role of mitonuclear interactions in population divergence and speciation.

Differential gene expression and mitonuclear incompatibilities in fast- and slow-developing inter-population Tigriopus californicus hybrids

“…Relatively few genes were differentially expressed between hybrids carrying a SD or SC mitochondrial genotype, which is unlike the substantial variation in nuclear gene expression associated with mitochondrial substitutions in Drosophila sp. (Mossman et al, 2016b(Mossman et al, , 2017(Mossman et al, , 2019 or differences in mitochondrial genotype in horseshoe bats (Rhinolophus affinis; Ding et al, 2021). However, modest effects of mitochondrial genotype on the transcriptome are observed in Atlantic killifish (Fundulus heteroclitus) from natural populations with genetic admixture between two subspecies (Flight et al, 2011;Healy et al, 2017), and only small numbers of genes are differentially expressed between T. californicus from the SD and SC populations (Barreto et al, 2015).…”

Mapping mitonuclear epistasis using a novel recombinant yeast population

“…Mitonuclear epistasis, defined as the non-additive phenotypic effects of interacting mitochondrial and nuclear allele pairs, has been demonstrated across Eukarya, including vertebrates [4][5][6], invertebrates [7][8][9][10][11][12], plants [13] and fungi [14][15][16][17][18][19][20][21]. In humans, allelic variation in mitonuclear interactions contributes to human diseases [22][23][24][25][26].…”

Mapping mitonuclear epistasis using a novel recombinant yeast population

“…Due to the low resolution of QTL mapping, specific loci were not identified, but in some cases, regions of mitonuclear genomic interest were implicated. Other approaches to uncovering mitonuclear epistatic loci include differential expression analysis [5, 39–41] and experimental evolution [42, 43]. Because relatively few genetic backgrounds are used for these mapping approaches, even if single gene pairs are identified, it is not clear if these approaches will reveal a general picture of mitonuclear epistasis or lineage specific idiosyncrasies.…”

“…Due to the low resolution of QTL mapping, specific loci were not identified, but in some cases, regions of mitonuclear genomic interest were implicated. Other approaches to uncovering mitonuclear epistatic loci include differential expression analysis [5,[39][40][41] and experimental evolution [42,43].…”

“…Genetic variation in natural systems can alter the efficiencies of these interactions leading to phenotypic differences between individuals and populations. Mitonuclear epistasis, defined as the non-additive phenotypic effects of interacting mitochondrial and nuclear allele pairs, has been demonstrated across Eukarya, including vertebrates [4][5][6], invertebrates [7][8][9][10][11][12], plants [13] and fungi [14][15][16][17][18][19][20]. In humans, allelic variation in mitonuclear interactions contributes to human diseases [21][22][23][24][25].…”