Selection on Mitochondrial Variants Occurs between and within Individuals in an Expanding Invasion

Rollins, Lee A.; Woolnough, Andrew P.; Fanson, Benjamin G.; Cummins, Michelle; Crowley, Tamsyn M.; Wilton, Alan N.; Sinclair, Ron; Butler, Ashleigh E.; Sherwin, William B.

doi:10.1093/molbev/msv343

Cited by 42 publications

(40 citation statements)

References 69 publications

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“…However, these types of methods have important limitations: they require data across multiple species, or sequences that are reasonably diverged, and only allow selection inference within coding regions (Gonçalves da Silva, 2017). It is important to consider this last limitation since mitonuclear incompatibilities have been mapped to non-coding regulatory genes, non-coding sequences such as transfer RNAs and the mitochondrial control region (Montooth et al, 2009; Meiklejohn et al, 2013; Rollins et al, 2016; Jhuang et al, 2017). …”

Section: Integrative Approaches For Studying Mitonuclear Co-evolutionmentioning

confidence: 99%

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

et al. 2017

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In animals, interactions among gene products of mitochondrial and nuclear genomes (mitonuclear interactions) are of profound fitness, evolutionary, and ecological significance. Most fundamentally, the oxidative phosphorylation (OXPHOS) complexes responsible for cellular bioenergetics are formed by the direct interactions of 13 mitochondrial-encoded and ∼80 nuclear-encoded protein subunits in most animals. It is expected that organisms will develop genomic architecture that facilitates co-adaptation of these mitonuclear interactions and enhances biochemical efficiency of OXPHOS complexes. In this perspective, we present principles and approaches to understanding the co-evolution of these interactions, with a novel focus on how genomic architecture might facilitate it. We advocate that recent interdisciplinary advances assist in the consolidation of links between genotype and phenotype. For example, advances in genomics allow us to unravel signatures of selection in mitochondrial and nuclear OXPHOS genes at population-relevant scales, while newly published complete atomic-resolution structures of the OXPHOS machinery enable more robust predictions of how these genes interact epistatically and co-evolutionarily. We use three case studies to show how integrative approaches have improved the understanding of mitonuclear interactions in OXPHOS, namely those driving high-altitude adaptation in bar-headed geese, allopatric population divergence in Tigriopus californicus copepods, and the genome architecture of nuclear genes coding for mitochondrial functions in the eastern yellow robin.

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Section: Integrative Approaches For Studying Mitonuclear Co-evolutionmentioning

confidence: 99%

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

et al. 2017

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“…Starlings are also an important species in invasion genetics research, due to their global introduction history 1, their invasion success and their known patterns of morphological and genetic variation across introduced ranges 2-4, making them ideal for studies of rapid evolution replicated across invasions. However, these studies require improved genetic resources.…”

Section: Introductionmentioning

confidence: 99%

“…Here we characterise the first starling transcriptome data set, produced using liver tissue from individuals sourced from the range edge in Western Australia and carrying genetic variants previously shown to be under selection 4. Two juvenile male starlings (S274, S290) were collected from Western Australia (S274: S 33.81542, E 120.95964; S290: S 33.79625, E 120.90078).…”

Section: Introductionmentioning

confidence: 99%

De Novo Assembly of the Liver Transcriptome of the European Starling, Sturnus vulgaris

Richardson¹,

Sherwin²,

Rollins³

2017

J. Genomics

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The European starling, Sturnus vulgaris, is a prolific and worldwide invasive species that also has served as an important model for avian ecological and invasion research. Although the genome sequence recently has become available, no transcriptome data have been published for this species. Here, we have sequenced and assembled the S. vulgaris liver transcriptome, which will provide a foundational resource for further annotation and validation of the draft genome. Moreover, it will be important for ecological and evolutionary studies investigating the genetic factors underlying rapid evolution and invasion success in this global invader.

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“…In addition to nonsynonymous point mutations, length variation due to insertion and deletion of tandem repeats has been found in control regions of insects, fish, mammals and plants and seems common within populations and even within individuals (heteroplasmy; Nishizawa, Kubo, & Mikami, ; Ravago, Monje, & Juinio‐Menez, ; Townsend & Rand, ; Wilkinson & Chapman, ). Although most variation in the control region is considered selectively neutral, substitutions may affect nucleotide synthesis (Fumagalli, Taberlet, Favre, & Hausser, ; Zhang & Hewitt, ) and mtDNA copy number (Butler et al, ). Through whole mitochondrial genome sequencing, we found variation in the number of tandem repeats in the control region in two samples, although this variation on its own did not seem to be strongly associated with haplotype fitness.…”

Section: Discussionmentioning

confidence: 99%

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

et al. 2019

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Despite the mitochondrion's long‐recognized role in energy production, mitochondrial DNA (mtDNA) variation commonly found in natural populations was assumed to be effectively neutral. However, variation in mtDNA has now been increasingly linked to phenotypic variation in life history traits and fitness. We examined whether the relative fitness in native and invasive common wasp (Vespula vulgaris) populations in Belgium and New Zealand (NZ), respectively, can be linked to mtDNA variation. Social wasp colonies in NZ were smaller with comparatively fewer queen cells, indicating a reduced relative fitness in the invaded range. Interestingly, queen cells in this population were significantly larger leading to larger queen offspring. By sequencing 1,872 bp of the mitochondrial genome, we determined mitochondrial haplotypes and detected reduced genetic diversity in NZ. Three common haplotypes in NZ frequently produced many queens, whereas the four rare haplotypes produced significantly fewer or no queens. The entire mitochondrial genome for each of these haplotypes was sequenced to identify polymorphisms associated with fitness reduction. We found 16 variable sites; however, no nonsynonymous mutation that was clearly causing impaired mitochondrial function was detected. We discuss how detected variants may alter secondary structures, gene expression or mito‐nuclear interactions, or could be associated with nuclear‐encoded variation. Whatever the ultimate mechanism, we show reduced fitness and mtDNA variation in an invasive wasp population as well as specific mtDNA variants associated with fitness variation within this population. Ours is one of only a few studies that confirm fitness impacts of mtDNA variation in wild nonmodel populations.

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Selection on Mitochondrial Variants Occurs between and within Individuals in an Expanding Invasion

Cited by 42 publications

References 69 publications

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

De Novo Assembly of the Liver Transcriptome of the European Starling, Sturnus vulgaris

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

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