Evolution and molecular bases of reproductive isolation

Bozdag, G. Ozan; Ono, Jasmine

doi:10.1016/j.gde.2022.101952

Cited by 10 publications

(11 citation statements)

References 76 publications

(91 reference statements)

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“…We have already noted examples of mitonuclear incompatibilities associated with direct physical interactions between mitochondrial gene products and imported nuclear-encoded proteins (Meiklejohn, et al 2013;Moran, et al 2021). These and similar examples have suggested that mitochondrial genes are frequent contributors to reproductive isolation and speciation (Burton and Barreto 2012;Hill 2016;Postel and Touzet 2020;Bozdag and Ono 2022). Meanwhile, many of the nuclear genes that have been implicated in BDMIs are involved in various forms of genomic conflict and antagonistic coevolution, including centromere binding, transposable element activity, male sterility, testis-specific functions, and pathogen defense (Johnson 2010;Crespi and Nosil 2013;Sankararaman, et al 2014;Serrato-Capuchina and Matute 2018;Postel and Touzet 2020;Schluter and Rieseberg 2022).…”

Section: Epistatic Incompatibilities Exposed By Hybridization and Hgtmentioning

confidence: 87%

“…Studies have also been increasingly successful in pinpointing examples of specific genes involved in postzygotic reproductive isolation in the form of so-called Bateson-Dobzhansky-Muller incompatibilities (BDMIs; Table 1) (Johnson 2010;Bozdag and Ono 2022). The growing list of these "speciation genes" is enriched for certain functional categories.…”

Section: Epistatic Incompatibilities Exposed By Hybridization and Hgtmentioning

confidence: 99%

“…This prediction arises from the following line of argument: 1) OXPHOS complexes are generally composed of both mitochondrialand nuclear-encoded subunits, 2) mitochondrial genomes experience higher mutation rates and more rapid sequence evolution than in the nucleus in many eukaryotes, and 3) nuclear genes may experience selection for coevolutionary responses to changes in interacting mitochondrial genes, resulting in co-adapted mitonuclear genotypes that are sensitive to disruption by hybridization. Analyses of evolutionary rates and signatures of selection have found indirect evidence of coevolution between mitochondrial-and nuclear-encoded subunits in these complexes (Osada and Akashi 2012;Havird, et al 2015;Neverov, et al 2021), and a number of nuclear-encoded proteins that function in other aspects of mitochondrial biology have been implicated in BDMIs (Table 1) Bozdag and Ono 2022). However, specific examples of incompatibilities arising from interactions within OXPHOS complexes have remained somewhat limited (Burton 2022).…”

Section: Multisubunit Complexes and Extent Of Protein-protein Interac...mentioning

confidence: 99%

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Incompatibility and interchangeability in molecular evolution

Sloan¹,

Warren²,

Williams³

et al. 2022

Preprint

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There is remarkable variation in the rate at which genetic incompatibilities in molecular interactions accumulate. In some cases, minor changes – even single nucleotide substitutions – create major epistatic incompatibilities when hybridization forces new variants to function in a novel genetic background from an isolated population. In other cases, genes or even entire functional pathways can be horizontally transferred between anciently divergent evolutionary lineages that span the tree of life with little evidence of incompatibilities. In this review, we explore whether there are general principles that can explain why certain genes are prone to epistatic incompatibilities while others maintain interchangeability. We summarize evidence pointing to four genetic features that may contribute to greater resistance to functional replacement: 1) function in multisubunit enzyme complexes and protein-protein interactions, 2) sensitivity to changes in gene dosage, 3) rapid rate of sequence evolution, and 4) overall importance to cell viability, which creates sensitivity to small perturbations in molecular function. We discuss the relative levels of support for these different hypotheses and lay out future directions that may help explain the striking contrasts in patterns of incompatibility and interchangeability throughout the history of molecular evolution.

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Section: Epistatic Incompatibilities Exposed By Hybridization and Hgtmentioning

confidence: 87%

Section: Epistatic Incompatibilities Exposed By Hybridization and Hgtmentioning

confidence: 99%

Section: Multisubunit Complexes and Extent Of Protein-protein Interac...mentioning

confidence: 99%

See 1 more Smart Citation

Incompatibility and interchangeability in molecular evolution

Sloan¹,

Warren²,

Williams³

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Studies have also been increasingly successful in pinpointing examples of specific genes involved in postzygotic reproductive isolation in the form of so-called Bateson–Dobzhansky–Muller incompatibilities (BDMIs; table 1 ; Johnson 2010 ; Bozdag and Ono 2022 ). These incompatibilities represent a form of epistasis in which two or more variants function without detrimental effects in their respective genetic backgrounds but have harmful interactions when brought together by hybridization.…”

Section: Genetic Incompatibilities Exposed By Hybridization and Hgtmentioning

confidence: 99%

Incompatibility and Interchangeability in Molecular Evolution

Sloan

Warren

Williams

et al. 2022

Genome Biology and Evolution

View full text Add to dashboard Cite

There is remarkable variation in the rate at which genetic incompatibilities in molecular interactions accumulate. In some cases, minor changes – even single nucleotide substitutions – create major incompatibilities when hybridization forces new variants to function in a novel genetic background from an isolated population. In other cases, genes or even entire functional pathways can be horizontally transferred between anciently divergent evolutionary lineages that span the tree of life with little evidence of incompatibilities. In this review, we explore whether there are general principles that can explain why certain genes are prone to incompatibilities while others maintain interchangeability. We summarize evidence pointing to four genetic features that may contribute to greater resistance to functional replacement: 1) function in multisubunit enzyme complexes and protein-protein interactions, 2) sensitivity to changes in gene dosage, 3) rapid rate of sequence evolution, and 4) overall importance to cell viability, which creates sensitivity to small perturbations in molecular function. We discuss the relative levels of support for these different hypotheses and lay out future directions that may help explain the striking contrasts in patterns of incompatibility and interchangeability throughout the history of molecular evolution.

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“…When genetically diverse individuals are crossed, they can produce hybrids that are sterile and/or present significant growth defects, depending on the degree of genetic incompatibility of their parents (Figure 2A). These incompatibilities can arise as a consequence of large-scale genome reorganization events such as aneuploidy, chromosomal rearrangements, or as a result of the parents' divergence in key cellular processes (Bozdag & Ono, 2022). The ease in mating and phenotypic analysis of yeast hybrids greatly facilitates dissecting the origins of molecular incompatibilities.…”

Section: Yeast Hybrids and Natural Isolatesmentioning

confidence: 99%

Experimental approaches to study evolutionary cell biology using yeasts

Natalino¹,

Fumasoni²

2022

Preprint

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The past century has witnessed tremendous advances in understanding how cells function. Nevertheless, how cellular processes have specifically evolved is still poorly understood. Many studies have highlighted surprising molecular diversity in how cells from various species execute the same processes, and advances in comparative genomics are likely to reveal much more molecular diversity than was believed possible until recently. Extant cells remain therefore the product of evolutionary history we vastly ignore. Evolutionary cell biology has emerged as a discipline aimed to address this knowledge gap by combining evolutionary, molecular, and cellular biology thinking. Recent studies have shown how even essential molecular processes, such as DNA replication, can undergo fast adaptive evolution under certain laboratory conditions. These approaches can open new lines of research where the evolution of cellular processes can be investigated experimentally. Yeasts naturally find themselves at the forefront of this research line. They not only allow us to observe fast evolutionary adaptation, but they also provide vast genomic, synthetic, and cellular biology tools previously developed by a large community. Here we propose that yeasts can serve as an ‘evolutionary cell lab’ to test hypotheses, principles, and ideas in evolutionary cell biology. We discuss various experimental approaches available for this purpose, and how biology at large can benefit from them.

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Evolution and molecular bases of reproductive isolation

Cited by 10 publications

References 76 publications

Incompatibility and interchangeability in molecular evolution

Incompatibility and interchangeability in molecular evolution

Incompatibility and Interchangeability in Molecular Evolution

Experimental approaches to study evolutionary cell biology using yeasts

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