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Abstract Mitochondrial functions are intimately reliant on proteins and RNAs encoded in both the nuclear and mitochondrial genomes, leading to inter‐genomic coevolution within taxa. Hybridization can break apart coevolved mitonuclear genotypes, resulting in decreased mitochondrial performance and reduced fitness. This hybrid breakdown is an important component of outbreeding depression and early‐stage reproductive isolation. However, the mechanisms contributing to mitonuclear interactions remain poorly resolved. Here, we scored variation in developmental rate (a proxy for fitness) among reciprocal F2interpopulation hybrids of the intertidal copepodTigriopus californicusand used RNA sequencing to assess differences in gene expression between fast‐ and slow‐developing hybrids. In total, differences in expression associated with developmental rate were detected for 2925 genes, whereas only 135 genes were differentially expressed as a result of differences in mitochondrial genotype. Upregulated expression in fast developers was enriched for genes involved in chitin‐based cuticle development, oxidation–reduction processes, hydrogen peroxide catabolic processes and mitochondrial respiratory chain complex I. In contrast, upregulation in slow developers was enriched for DNA replication, cell division, DNA damage and DNA repair. Eighty‐four nuclear‐encoded mitochondrial genes were differentially expressed between fast‐ and slow‐developing copepods, including 12 subunits of the electron transport system (ETS) which all had higher expression in fast developers than in slow developers. Nine of these genes were subunits of ETS complex I. Our results emphasize the major roles that mitonuclear interactions within the ETS, particularly in complex I, play in hybrid breakdown, and resolve strong candidate genes for involvement in mitonuclear interactions.
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Absence of heterosis for hypoxia tolerance in F1 hybrids of Tigriopus californicus
Abstract Hybridization produces a range of outcomes from advantageous to disadvantageous, and a goal of genetic research is to understand the gene interactions that generate these outcomes. Interactions between cytoplasmic elements, such as mitochondria, and the nucleus may be particularly vulnerable to accruing disadvantageous combinations as a result of their different rates of evolution. Consequently, mitonuclear incompatibilities may play an important role in hybrid outcomes even if their negative impacts could be masked for some fitness measures by heterosis in first-generation (F1) hybrids. We used Tigriopus californicus, a model system for mitonuclear incompatibilities that is also known for exhibiting heterosis in the F1 generation and outbreeding depression in later generations, to test whether heterosis or outbreeding depression would occur when mitonuclear mismatch was paired with a stress that heavily impacts mitochondrial processes—specifically, hypoxia. We generated 284 parental and 436 F1 hybrids from four population crosses (720 total) and compared parental and F1 populations for hypoxia tolerance. We observed that, on average, F1 hybrids were less likely to survive a hypoxia stress test than parental populations, although we did not detect a statistically significant trend (P = 0.246 to 0.614). This suggests that hypoxia may be a particularly intense stressor for mitonuclear coordination and hybridization outcomes vary by trait.
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- Award ID(s):
- 2029156
- PAR ID:
- 10630499
- Editor(s):
- Delmore, Kira
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Heredity
- Volume:
- 116
- Issue:
- 2
- ISSN:
- 0022-1503
- Page Range / eLocation ID:
- 149 to 158
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract All mitochondrial-encoded proteins and RNAs function through interactions with nuclear-encoded proteins, which are critical for mitochondrial performance and eukaryotic fitness. Coevolution maintains inter-genomic (i.e., mitonuclear) compatibility within a taxon, but hybridization can disrupt coevolved interactions, resulting in hybrid breakdown. Thus, mitonuclear incompatibilities may be important mechanisms underlying reproductive isolation and, potentially, speciation. Here we utilize Pool-seq to assess the effects of mitochondrial genotype on nuclear allele frequencies in fast- and slow-developing reciprocal inter-population F2 hybrids between relatively low-divergence populations of the intertidal copepod Tigriopus californicus. We show that mitonuclear interactions lead to elevated frequencies of coevolved (i.e., maternal) nuclear alleles on two chromosomes in crosses between populations with 1.5% or 9.6% fixed differences in mitochondrial DNA nucleotide sequence. However, we also find evidence of excess mismatched (i.e., noncoevolved) alleles on three or four chromosomes per cross, respectively, and of allele frequency differences consistent with effects involving only nuclear loci (i.e., unaffected by mitochondrial genotype). Thus, our results for low-divergence crosses suggest an underlying role for mitonuclear interactions in variation in hybrid developmental rate, but despite substantial effects of mitonuclear coevolution on individual chromosomes, no clear bias favoring coevolved interactions overall.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/jhered/esae061
