Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages

Lavrov, Dennis V.; Pett, Walker

doi:10.1093/gbe/evw195

Cited by 172 publications

(203 citation statements)

References 236 publications

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“…In most bilaterian animals, mutation rates in the mtDNA outstrip those in the nucleus (Lavrov and Pett 2016). In most angiosperms, the opposite is true (Wolfe et al.…”

Section: Discussionmentioning

confidence: 99%

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

Havird

Trapp

Miller

et al. 2017

Genome Biology and Evolution

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Understanding mechanisms of coevolution between nuclear and mitochondrial (mt) genomes is a defining challenge in eukaryotic genetics. The angiosperm genus Silene is a natural system to investigate the causes and consequences of mt mutation rate variation because closely related species have highly divergent rates. In Silene species with fast-evolving mtDNA, nuclear genes that encode mitochondrially targeted proteins (N-mt genes) are also fast-evolving. This correlation could indicate positive selection to compensate for mt mutations, but might also result from a recent relaxation of selection. To differentiate between these interpretations, we used phylogenetic and population-genetic methods to test for positive and relaxed selection in three classes of N-mt genes (oxidative phosphorylation genes, ribosomal genes, and “RRR” genes involved in mtDNA recombination, replication, and repair). In all three classes, we found that species with fast-evolving mtDNA had: 1) elevated dN/dS, 2) an excess of nonsynonymous divergence relative to levels of intraspecific polymorphism, which is a signature of positive selection, and 3) no clear signals of relaxed selection. “Control” genes exhibited comparatively few signs of positive selection. These results suggest that high mt mutation rates can create selection on N-mt genes and that relaxed selection is an unlikely cause of recent accelerations in the evolution of N-mt genes. Because mt-RRR genes were found to be under positive selection, it is unlikely that elevated mt mutation rates in Silene were caused by inactivation of these mt-RRR genes. Therefore, the causes of extreme increases in angiosperm mt mutation rates remain uncertain.

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“…In most bilaterian animals, mutation rates in the mtDNA outstrip those in the nucleus (Lavrov and Pett 2016). In most angiosperms, the opposite is true (Wolfe et al.…”

Section: Discussionmentioning

confidence: 99%

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

Havird

Trapp

Miller

et al. 2017

Genome Biology and Evolution

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“…Sequences were aligned with MAFFT (E‐ INS ‐i), and divergent N‐ and C‐terminal portions of the alignment were manually trimmed. Branch length estimates were then generated in PAML v4.9a, using an LG +G model and a topology that was constrained based on published sources (Burki ; Lavrov & Pett ).…”

Section: Deleterious Mutation Accumulation and The Efficacy Of Selectmentioning

confidence: 98%

“…Sequences were aligned with MAFFT (E-INS-i), and divergent N-and C-terminal portions of the alignment were manually trimmed. Branch length estimates were then generated in PAML v4.9a, using an LG+G model and a topology that was constrained based on published sources (Burki 2014;Lavrov & Pett 2016). of eukaryotic species or specific regions of eukaryotic genomes (e.g. Y chromosomes) that have transitioned to asexual modes of inheritance (Kaiser & Charlesworth 2010;Neiman et al 2010;Tucker et al 2013;Hollister et al 2015;Sharbrough et al 2016).…”

Section: Empirical Evidence For Deleterious Mutation Accumulation In mentioning

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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“…However, variation in gene content has been frequently reported in animal mitogenomes, including loss and/or gain of PCGs, rRNAs, and/or tRNAs (Gissi, Iannelli, & Pesole, 2008;Lavrov & Pett, 2016 Interestingly, trnI was present in the mitogenome of the congeneric C. septempunctata. Generally, gene content in each mitogenome is highly conserved in most animals.…”

Section: Characteristics Of Mitochondrial Genomes In Coccinellidaementioning

confidence: 99%

Mitogenome evolution in ladybirds: Potential association with dietary adaptation

Yüan

Zhang

et al. 2020

Ecology and Evolution

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Dietary shifts can alter the relative availability of different nutrients and are therefore associated with metabolic adaptation in animals. The Coccinellidae (ladybirds) exhibits three major types of feeding habits and provides a useful model to study the effects of dietary changes on the evolution of mitogenomes, which encode proteins directly involved in energy metabolism. Here, mitogenomes of three coccinellid species were newly sequenced. These data were combined with other ten previously sequenced coccinellid mitogenomes to explore the relationship between mitogenome evolution and diets. Our results indicate that mitogenomic data can be effectively used to resolve phylogenetic relationships of Coccinellidae. Strong codon usage bias in coccinellid mitogenomes was predominantly determined by nucleotide composition. The 13 mitochondrial protein-coding genes (PCGs) globally evolved under negative constraints, with some PCGs showing a stronger purifying selection. Six PCGs (nad3, nad4L, and nad5 from Complex I; cox1 and cox3 from Complex IV; and atp6 from Complex V) displayed signs of positive selection. Of these, adaptive changes in cox3 were potentially associated with metabolic differences resulting from dietary shifts in Coccinellidae. Our results provide insights into the adaptive evolution of coccinellid mitogenomes in response to both dietary shifts and other life history traits. K E Y W O R D S diet evolution, mitochondrial DNA, molecular phylogeny, negative selection, positive selection | 1043 YUAN et Al.

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Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages

Cited by 172 publications

References 236 publications

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

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

Mitogenome evolution in ladybirds: Potential association with dietary adaptation

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