Incompatibility of Nuclear and Mitochondrial Genomes Causes Hybrid Sterility between Two Yeast Species

Lee, Hsin‐Yi; Chou, Jui-Yu; Cheong, Liplee; Chang, Nai-Hsin; Yang, Shi-Yow; Leu, Jun‐Yi

doi:10.1016/j.cell.2008.10.047

Cited by 329 publications

(381 citation statements)

References 35 publications

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“…In a laboratory experiment, Dettman et al (31) recorded intrinsic postzygotic isolation affecting growth rate and frequency of meiosis in hybrids between yeast populations that had evolved for 500 generations in 2 distinct environments. Without more evidence on the mechanism of selection we are unable to determine which, if any, of the genes recently discovered to underlie intrinsic postzygotic isolation in Drosophila, yeast, and mice (5,(32)(33)(34)(35) fixed as a result of ecologically-based divergent natural selection.…”

Section: Divergent Selection and Postzygotic Isolationmentioning

confidence: 99%

Genetics and ecological speciation

Schluter

Conte

2009

Proc. Natl. Acad. Sci. U.S.A.

557

616

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Species originate frequently by natural selection. A general mechanism by which this occurs is ecological speciation, defined as the evolution of reproductive isolation between populations as a result of ecologically-based divergent natural selection. The alternative mechanism is mutation-order speciation in which populations fix different mutations as they adapt to similar selection pressures. Although numerous cases now indicate the importance of ecological speciation in nature, very little is known about the genetics of the process. Here, we summarize the genetics of premating and postzygotic isolation and the role of standing genetic variation in ecological speciation. We discuss the role of selection from standing genetic variation in threespine stickleback (Gasterosteus aculeatus), a complex of species whose ancestral marine form repeatedly colonized and adapted to freshwater environments. We propose that ecological speciation has occurred multiple times in parallel in this group via a ''transporter'' process in which selection in freshwater environments repeatedly acts on standing genetic variation that is maintained in marine populations by export of freshwater-adapted alleles from elsewhere in the range. Selection from standing genetic variation is likely to play a large role in ecological speciation, which may partly account for its rapidity.reproductive isolation ͉ stickleback ͉ standing genetic variation ͉ transporter hypothesis O ne of Darwin's greatest ideas was that new species originate by natural selection (1). It has taken evolutionary biologists almost until now to realize that he was probably correct. Darwin looked at species mainly as sets of individuals closely resembling each other (1), in which case adaptive divergence in phenotype eventually leads to speciation almost by definition. Later, Dobzhansky (2) and Mayr (3) defined species and speciation by the criterion of reproductive isolation instead. Recent evidence indicates that reproductive isolation also evolves frequently by natural selection (4-7).Speciation by natural selection occurs by 2 general mechanisms (4, 7). The first of these is ecological speciation, defined as the evolution of reproductive isolation between populations, or subsets of a single population, as a result of ecologically-based divergent natural selection (6,(8)(9)(10). Under this process natural selection acts in contrasting directions between environments, which drives the fixation of different alleles each advantageous in one environment but not in the other (Fig. 1). In contrast, under mutation-order speciation (7, 11), populations diverge as they accumulate a different series of mutations under similar selection pressures (Fig. 1). Natural selection drives alleles to fixation in both speciation mechanisms, but selection favors divergence only under ecological speciation. Divergence occurs by chance under the mutation-order process.There is growing evidence in support of both ecological and mutation-order speciation in nature (4, 7), yet numerous aspects of ...

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Section: Divergent Selection and Postzygotic Isolationmentioning

confidence: 99%

Genetics and ecological speciation

Schluter

Conte

2009

Proc. Natl. Acad. Sci. U.S.A.

557

616

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“…This work strongly suggests that the poor performance is linked to altered binding motifs of the transcription system establishing contact between POLRMT and mtDNA that have coevolved with their counterpart mtDNA recognition sites between the two species [70,87]. Another such example comes from a yeast hybrid model between Saccharomyces cerevisiae and Saccharomyces bayanus identifying the inability of the nuclear translation factor AEP2 (S. bayanus) to regulate the translation of the mitochondrial F0-ATP synthase subunit c (OLI1, S. cerevisiae), causing sterility and sporulation defects [88,89]. Similar translational breakdown between species was observed between hybrids of S. cerevisiae, S. bayanus or Saccharomyces paradoxis, revealing the inability to properly splice mtDNA-encoded COX1 via the interaction with the nuclear factor Mrs1, thus leading to sterility [89].…”

Section: Interspecies 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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“…DNA sequence divergence and expression levels of sex-related genes in many studies support the idea that genes involved in male fertility diverge faster between species than other types of genes . Hybrid sterility-causative genes, such as Odysseus site homeobox (OdsH) in Drosophila (Ting et al, 1998), Meisetz (Prdm9) in mice (Oliver et al, 2009) and AEP2/OLI1 in yeast (Lee et al, 2008), are often characterized by rapid sequence evolution and distinct expression patterns. Candidate genes for speciation, therefore, include genes responsible for spermatogenesis and sperm motility and other genes that cause reproductive incompatibilities in hybrids.…”

Section: Introductionmentioning

confidence: 99%

Hybrid sterility and evolution in Hawaiian Drosophila: differential gene and allele-specific expression analysis of backcross males

et al. 2016

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The Hawaiian Drosophila are an iconic example of sequential colonization, adaptive radiation and speciation on islands. Genetic and phenotypic analysis of closely related species pairs that exhibit incomplete reproductive isolation can provide insights into the mechanisms of speciation. Drosophila silvestris from Hawai'i Island and Drosophila planitibia from Maui are two closely related allopatric Hawaiian picture-winged Drosophila that produce sterile F 1 males but fertile F 1 females, a pattern consistent with Haldane's rule. Backcrossing F 1 hybrid females between these two species to parental species gives rise to recombinant males with three distinct sperm phenotypes despite a similar genomic background: motile sperm, no sperm (sterile), and immotile sperm. We found that these three reproductive morphologies of backcross hybrid males produce divergent gene expression profiles in testes, as measured with RNA sequencing. There were a total of 71 genes significantly differentially expressed between backcross males with no sperm compared with those backcross males with motile sperm and immotile sperm, but no significant differential gene expression between backcross males with motile sperm and backcross males with immotile sperm. All of these genes were underexpressed in males with no sperm, including a number of genes with previously known activities in adult testis. An allele-specific expression analysis showed overwhelmingly more cis-divergent than transdivergent genes, with no significant difference in the ratio of cis-and trans-divergent genes among the sperm phenotypes. Overall, the results indicate that the regulation of gene expression involved in sperm production likely diverged relatively rapidly between these two closely related species.

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Incompatibility of Nuclear and Mitochondrial Genomes Causes Hybrid Sterility between Two Yeast Species

Cited by 329 publications

References 35 publications

Genetics and ecological speciation

Genetics and ecological speciation

Mitonuclear interactions: evolutionary consequences over multiple biological scales

Hybrid sterility and evolution in Hawaiian Drosophila: differential gene and allele-specific expression analysis of backcross males

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