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Abstract BackgroundMitochondrial genes and nuclear genes cooperate closely to maintain the functions of mitochondria, especially in the oxidative phosphorylation (OXPHOS) pathway. However, mitochondrial genes among arthropod lineages have dramatic evolutionary rate differences. Haplodiploid arthropods often show fast-evolving mitochondrial genes. One hypothesis predicts that the small effective population size of haplodiploid species could enhance the effect of genetic drift leading to higher substitution rates in mitochondrial and nuclear genes. Alternatively, positive selection or compensatory changes in nuclear OXPHOS genes could lead to the fast-evolving mitochondrial genes. However, due to the limited number of arthropod genomes, the rates of evolution for nuclear genes in haplodiploid species, besides hymenopterans, are largely unknown. To test these hypotheses, we used data from 76 arthropod genomes, including 5 independently evolved haplodiploid lineages, to estimate the evolutionary rates and patterns of gene family turnover of mitochondrial and nuclear genes. ResultsWe show that five haplodiploid lineages tested here have fast-evolving mitochondrial genes and fast-evolving nuclear genes related to mitochondrial functions, while nuclear genes not related to mitochondrion showed no significant evolutionary rate differences. Among hymenopterans, bees and ants show faster rates of molecular evolution in mitochondrial genes and mitochondrion-related nuclear genes than sawflies and wasps. With genome data, we also find gene family expansions and contractions in mitochondrion-related genes of bees and ants. ConclusionsOur results reject the small population size hypothesis in haplodiploid species. A combination of positive selection and compensatory changes could lead to the observed patterns in haplodiploid species. The elevated evolutionary rates in OXPHOS complex 2 genes of bees and ants suggest a unique evolutionary history of social hymenopterans.
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Can transcriptome size and off-target effects explain the contrasting evolution of mitochondrial vs nuclear RNA editing?
Abstract Mitochondrial RNA editing has evolved independently in numerous eukaryotic lineages, where it generally restores conserved sequences and functional reading frames in mRNA transcripts derived from altered or disrupted mitochondrial protein-coding genes. In contrast to this “restorative” RNA editing in mitochondria, most editing of nuclear mRNAs introduces novel sequence variants and diversifies the proteome. This Perspective addresses the hypothesis that these completely opposite effects of mitochondrial vs. nuclear RNA editing arise from the enormous difference in gene number between the respective genomes. Because mitochondria produce a much smaller transcriptome, they likely create less opportunity for off-target editing, which has been supported by recent experimental work expressing mitochondrial RNA editing machinery in foreign contexts. In addition, there is recent evidence that the size and complexity of RNA targets may slow the kinetics and reduce efficiency of on-target RNA editing. These findings suggest that efficient targeting and a low risk of off-target editing have facilitated the repeated emergence of disrupted mitochondrial genes and associated restorative RNA editing systems via (potentially non-adaptive) evolutionary pathways that are not feasible in larger nuclear transcriptomes due to lack of precision.
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- Award ID(s):
- 2048407
- PAR ID:
- 10652679
- Editor(s):
- Meisel, Richard; Pozzi, Andrea
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- ISSN:
- 1420-9101
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/jeb/voaf042
