Tracing Hybrid Incompatibilities to Single Amino Acid Substitutions

Harrison, J. Scott; Burton, Ronald S.

doi:10.1093/molbev/msj058

Cited by 98 publications

(99 citation statements)

References 25 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Such hybridization results in fitness breakdown in the F 2 generation, marked by decreased survivorship of larvae [62], slower development [63], reduced fecundity and viability [64], as well as decreased cyclooxygenase (COX) activity and ATP production [64][65][66]. The decrease in COX activity and ATP production is plausibly triggered by a set of mutations in the mitochondrial cytochrome c [67,68]. These mtDNA mutations appear to be compensated by restorer counter-adaptations within the population-specific coevolved nuclear backgrounds, which become 'unmasked' in F 2 hybrids [68].…”

Section: Interpopulation Interactionsmentioning

confidence: 99%

“…The decrease in COX activity and ATP production is plausibly triggered by a set of mutations in the mitochondrial cytochrome c [67,68]. These mtDNA mutations appear to be compensated by restorer counter-adaptations within the population-specific coevolved nuclear backgrounds, which become 'unmasked' in F 2 hybrids [68]. Reduced fitness of interpopulation hybrids in this model is further correlated with elevated oxidative damage [69], and associated with differential expression of mitochondrial and nuclear OXPHOS genes [70], indicating the complexity of consequences triggered by the disruption of the coevolved mitonuclear lineages.…”

Section: Interpopulation Interactionsmentioning

confidence: 99%

See 1 more Smart Citation

Mitonuclear interactions: evolutionary consequences over multiple biological scales

Wolff

Ladoukakis

Enrı́quez

et al. 2014

Phil. Trans. R. Soc. B

204

218

View full text Add to dashboard Cite

Fundamental biological processes hinge on coordinated interactions between genes spanning two obligate genomes—mitochondrial and nuclear. These interactions are key to complex life, and allelic variation that accumulates and persists at the loci embroiled in such intergenomic interactions should therefore be subjected to intense selection to maintain integrity of the mitochondrial electron transport system. Here, we compile evidence that suggests that mitochondrial–nuclear (mitonuclear) allelic interactions are evolutionarily significant modulators of the expression of key health-related and life-history phenotypes, across several biological scales—within species (intra- and interpopulational) and between species. We then introduce a new frontier for the study of mitonuclear interactions—those that occur within individuals, and are fuelled by the mtDNA heteroplasmy and the existence of nuclear-encoded mitochondrial gene duplicates and isoforms. Empirical evidence supports the idea of high-resolution tissue- and environment-specific modulation of intraindividual mitonuclear interactions. Predicting the penetrance, severity and expression patterns of mtDNA-induced mitochondrial diseases remains a conundrum. We contend that a deeper understanding of the dynamics and ramifications of mitonuclear interactions, across all biological levels, will provide key insights that tangibly advance our understanding, not only of core evolutionary processes, but also of the complex genetics underlying human mitochondrial disease.

show abstract

Section: Interpopulation Interactionsmentioning

confidence: 99%

Section: Interpopulation Interactionsmentioning

confidence: 99%

Mitonuclear interactions: evolutionary consequences over multiple biological scales

Wolff

Ladoukakis

Enrı́quez

et al. 2014

Phil. Trans. R. Soc. B

204

218

View full text Add to dashboard Cite

show abstract

“…In angiosperms, hybrid male sterility is thought to result frequently from negative epistatic interactions between cytoplasmic (most probably mitochondrial) and nuclear genes in interspecific hybrids (Frank 1989;Schnable and Wise 1998). Negative cytonuclear interactions are also known to contribute to reproductive isolation between animal species and even populations, where they have been identified as the genetic basis of both hybrid inviability and infertility ½e.g., Tigriopus (Willett and Burton 2001;Harrison and Burton 2006) and Drosophila (Rand et al 2001;Sackton et al 2003). Assuming uniparental inheritance of the relevant organelle, cytonuclear interactions involve interactions between a cytoplasmic genome from one parent (usually maternal, Grun 1976) and the genes in the hybrid nuclear genome derived from the second parent.…”

Section: Classes Of Asymmetric Genetic Interactionsmentioning

confidence: 99%

Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule

2007

View full text Add to dashboard Cite

Asymmetric postmating isolation, where reciprocal interspecific crosses produce different levels of fertilization success or hybrid sterility/inviability, is very common. Darwin emphasized its pervasiveness in plants, but it occurs in all taxa assayed. This asymmetry often results from Dobzhansky-Muller incompatibilities (DMIs) involving uniparentally inherited genetic factors (e.g., gametophyte-sporophyte interactions in plants or cytoplasmic-nuclear interactions). Typically, unidirectional (U) DMIs act simultaneously with bidirectional (B) DMIs between autosomal loci that affect reciprocal crosses equally. We model both classes of two-locus DMIs to make quantitative and qualitative predictions concerning patterns of isolation asymmetry in parental species crosses and in the hybrid F 1 generation. First, we find conditions that produce expected differences. Second, we present a stochastic analysis of DMI accumulation to predict probable levels of asymmetry as divergence time increases. We find that systematic interspecific differences in relative rates of evolution for autosomal vs. nonautosomal loci can lead to different expected F 1 fitnesses from reciprocal crosses, but asymmetries are more simply explained by stochastic differences in the accumulation of U DMIs. The magnitude of asymmetry depends primarily on the cumulative effects of U vs. B DMIs (which depend on heterozygous effects of DMIs), the average number of DMIs required to produce complete reproductive isolation (more asymmetry occurs when fewer DMIs are required), and the shape of the function describing how fitness declines as DMIs accumulate. Comparing our predictions to data from diverse taxa indicates that unidirectional DMIs, specifically involving sex chromosomes, cytoplasmic elements, and maternal effects, are likely to play an important role in postmating isolation.The degree of sterility does not strictly follow systematic affinity, but is governed by several curious and complex laws. It is generally different, and sometimes wildly different, in reciprocal crosses between the same two species. Darwin (1859)

show abstract

“…2014; Hill 2015), but cytochrome c oxidase (complex IV) and cytochrome c are frequently implicated in incompatibilities (Rawson and Burton 2002; Sackton et al. 2003; Harrison and Burton 2006). The key point for exploring the connections between a mitochondrial DNA barcode and the process of speciation is that mitochondrial genes often play a central role in hybrid incompatibilities (Gershoni et al.…”

Section: Introductionmentioning

confidence: 99%

Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap

Hill

2016

Ecology and Evolution

149

178

View full text Add to dashboard Cite

Mitochondrial genes are widely used in taxonomy and systematics because high mutation rates lead to rapid sequence divergence and because such changes have long been assumed to be neutral with respect to function. In particular, the nucleotide sequence of the mitochondrial gene cytochrome c oxidase subunit 1 has been established as a highly effective DNA barcode for diagnosing the species boundaries of animals. Rarely considered in discussions of mitochondrial evolution in the context of systematics, speciation, or DNA barcodes, however, is the genomic architecture of the eukaryotes: Mitochondrial and nuclear genes must function in tight coordination to produce the complexes of the electron transport chain and enable cellular respiration. Coadaptation of these interacting gene products is essential for organism function. I extend the hypothesis that mitonuclear interactions are integral to the process of speciation. To maintain mitonuclear coadaptation, nuclear genes, which code for proteins in mitochondria that cofunction with the products of mitochondrial genes, must coevolve with rapidly changing mitochondrial genes. Mitonuclear coevolution in isolated populations leads to speciation because population‐specific mitonuclear coadaptations create between‐population mitonuclear incompatibilities and hence barriers to gene flow between populations. In addition, selection for adaptive divergence of products of mitochondrial genes, particularly in response to climate or altitude, can lead to rapid fixation of novel mitochondrial genotypes between populations and consequently to disruption in gene flow between populations as the initiating step in animal speciation. By this model, the defining characteristic of a metazoan species is a coadapted mitonuclear genotype that is incompatible with the coadapted mitochondrial and nuclear genotype of any other population.

show abstract

Tracing Hybrid Incompatibilities to Single Amino Acid Substitutions

Cited by 98 publications

References 25 publications

Mitonuclear interactions: evolutionary consequences over multiple biological scales

Mitonuclear interactions: evolutionary consequences over multiple biological scales

Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule

Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap

Contact Info

Product

Resources

About