Interpopulation Hybrid Breakdown Maps to the Mitochondrial Genome

Ellison, Christopher K.; Burton, Ronald S.

doi:10.1111/j.1558-5646.2007.00305.x

Cited by 236 publications

(284 citation statements)

References 40 publications

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“…This is precisely what is seen in Tigriopus californicus, where crosses between any two populations are fully compatible (IPI index of 0), unidirectionally compatible (IPI index of 0.5) or fully incompatible (IPI index of 1), in which case F 1 hybrids of both sexes are sterile in one direction and inviable in the other 33,34 . Such a pattern indicates that uniparentally inherited factors (likely cyto-nuclear incompatibilities in this case 35 ) may be of special importance for the formation of IPI in taxa without sex chromosomes.…”

Section: Discussionmentioning

confidence: 99%

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

Lima

2014

Nat Commun

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The two 'rules of speciation', Haldane's rule and the large X-effect, describe the genetic basis of postzygotic isolation, and have led to the realization that sex chromosomes play an important role in this process. However, a range of sex determination mechanisms exists in nature, not always involving sex chromosomes. Based on these 'rules of speciation', I test the hypothesis that the presence of sex chromosomes will contribute to a faster evolution of intrinsic postzygotic isolation. I show that taxa that do not have sex chromosomes evolve lower levels of postzygotic isolation than taxa with sex chromosomes, at a similar amount of genetic divergence. Taxa with young homomorphic sex chromosomes show an intermediate pattern compared to taxa with heteromorphic sex chromosomes and taxa without sex chromosomes. These results are consistent with predictions from the two 'rules of speciation', and emphasize the importance of sex chromosomes for the evolution of intrinsic postzygotic isolation.

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Section: Discussionmentioning

confidence: 99%

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

Lima

2014

Nat Commun

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“…In marine copepods Tigriopus californicus , crossing animals from geographically isolated populations resulted in a 40% loss of ATP production in F2 population hybrids (Ellison and Burton 2006; Burton et al. 2013), with fitness loss linked specifically to loss of function in complexes I, III, and IV of the ETC due to incompatibilities between maternal mt genes and paternal N‐mt genes (Ellison and Burton 2008). Similar mitonuclear incompatibilities with loss of fitness have been observed in carefully manipulated hybrid crosses in Drosophila (Sackton 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

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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.

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“…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. Fitness of these hybrids can be restored via backcrossing to the maternal, not paternal, populations of origin, heavily implicating negative mitonuclear epistasis as the driver of the hybrid breakdown [71]. The impairment of fundamental functions-foremost the rstb.royalsocietypublishing.org Phil.…”

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

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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.

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Interpopulation Hybrid Breakdown Maps to the Mitochondrial Genome

Cited by 236 publications

References 40 publications

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

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

Mitonuclear interactions: evolutionary consequences over multiple biological scales

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