scholarly journals Hybrid incompatibility caused by an epiallele

2017 ◽  
Author(s):  
Todd Blevins ◽  
Jing Wang ◽  
David Pflieger ◽  
Frédéric Pontvianne ◽  
Craig S. Pikaard

AbstractHybrid incompatibility resulting from deleterious gene combinations is thought to be an important step towards reproductive isolation and speciation. Here we demonstrate involvement of a silent epiallele in hybrid incompatibility. In Arabidopsis thaliana strain Col-0, one of the two copies of a duplicated histidine biosynthesis gene, HISN6B is not expressed, for reasons that have been unclear, making its paralog, HISN6A essential. By contrast, in strain Cvi-0, HISN6B is essential because HISN6A is mutated. As a result of these differences, Cvi-0 × Col-0 hybrid progeny that are homozygous for both Col-0 HISN6B and Cvi-0 HISN6A do not survive. We show that HISN6B is not a defective pseudogene in the Col-0 strain, but a stably silenced epiallele. Mutating HISTONE DEACETYLASE 6 (HDA6) or the cytosine methyltransferase genes, MET1 or CMT3 erases HISN6B’s silent locus identity in Col-0, reanimating the gene such that hisn6a lethality and hybrid incompatibility are circumvented. These results show that HISN6-dependent hybrid lethality is a revertible epigenetic phenomenon and provide additional evidence that epigenetic variation has the potential to limit gene flow between diverging populations of a species.Significance statementDeleterious mutations in different copies of a duplicated gene pair have the potential to cause hybrid incompatibility between diverging subpopulations, contributing to reproductive isolation and speciation. This study demonstrates a case of epigenetic gene silencing, rather than pseudogene creation by mutation, contributing to a lethal gene combination upon hybridization of two strains of Arabidopsis thaliana. The findings provide direct evidence that naturally occurring epigenetic variation can contribute to incompatible hybrid genotypes, reducing gene flow between strains of the same species.

2017 ◽  
Vol 114 (14) ◽  
pp. 3702-3707 ◽  
Author(s):  
Todd Blevins ◽  
Jing Wang ◽  
David Pflieger ◽  
Frédéric Pontvianne ◽  
Craig S. Pikaard

Hybrid incompatibility resulting from deleterious gene combinations is thought to be an important step toward reproductive isolation and speciation. Here, we demonstrate involvement of a silent epiallele in hybrid incompatibility. In Arabidopsis thaliana accession Cvi-0, one of the two copies of a duplicated histidine biosynthesis gene, HISN6A, is mutated, making HISN6B essential. In contrast, in accession Col-0, HISN6A is essential because HISN6B is not expressed. Owing to these differences, Cvi-0 × Col-0 hybrid progeny that are homozygous for both Cvi-0 HISN6A and Col-0 HISN6B do not survive. We show that HISN6B of Col-0 is not a defective pseudogene, but a stably silenced epiallele. Mutating HISTONE DEACETYLASE 6 (HDA6), or the cytosine methyltransferase genes MET1 or CMT3, erases HISN6B's silent locus identity, reanimating the gene to circumvent hisn6a lethality and hybrid incompatibility. These results show that HISN6-dependent hybrid lethality is a revertible epigenetic phenomenon and provide additional evidence that epigenetic variation has the potential to limit gene flow between diverging populations of a species.


2019 ◽  
Vol 128 (3) ◽  
pp. 583-591
Author(s):  
Leo Joseph ◽  
Alex Drew ◽  
Ian J Mason ◽  
Jeffrey L Peters

Abstract We reassessed whether two parapatric non-sister Australian honeyeater species (Aves: Meliphagidae), varied and mangrove honeyeaters (Gavicalis versicolor and G. fasciogularis, respectively), that diverged from a common ancestor c. 2.5 Mya intergrade in the Townsville area of north-eastern Queensland. Consistent with a previous specimen-based study, by using genomics methods we show one-way gene flow for autosomal but not Z-linked markers from varied into mangrove honeyeaters. Introgression barely extends south of the area of parapatry in and around the city of Townsville. While demonstrating the long-term porosity of species boundaries over several million years, our data also suggest a clear role of sex chromosomes in maintaining reproductive isolation.


2014 ◽  
Author(s):  
Tiago Paixão ◽  
Kevin E. Bassler ◽  
Ricardo B. R. Azevedo

The Dobzhansky-Muller model posits that incompatibilities between alleles at different loci cause speciation. However, it is known that if the alleles involved in a Dobzhansky-Muller incompatibility (DMI) between two loci are neutral, the resulting reproductive isolation cannot be maintained in the presence of either mutation or gene flow. Here we show that speciation can emerge through the collective effects of multiple neutral DMIs that cannot, individually, cause speciation-a mechanism we call emergent speciation. We investigate emergent speciation using models of haploid holey adaptive landscapes-neutral networks-with recombination. We find that certain combinations of multiple neutral DMIs can lead to speciation. Furthermore, emergent speciation is a robust mechanism that can occur in the presence of migration, and of deviations from the assumptions of the neutral network model. Strong recombination and complex interactions between the DMI loci facilitate emergent speciation. These conditions are likely to occur in nature. We conclude that the interaction between DMIs may cause speciation.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190532 ◽  
Author(s):  
Alexandre Blanckaert ◽  
Claudia Bank ◽  
Joachim Hermisson

Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky–Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that many incipient species may initially face. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.


2002 ◽  
Vol 357 (1420) ◽  
pp. 471-492 ◽  
Author(s):  
Michele Drès ◽  
James Mallet

The existence of a continuous array of sympatric biotypes—from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species—can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant–feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca . 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one–half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by–product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host–associated polymorphism to host–associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite–resistant plants.


Behaviour ◽  
1995 ◽  
Vol 132 (15-16) ◽  
pp. 1173-1181 ◽  
Author(s):  
Valery V. Ziuganov

AbstractReproductive isolation was investigated among sympatric lateral plate morphs of threespine stickleback from the White Sea basin and also among phenotypically similar morphs from the distant Kamchatka River basin (Lake Azabachije). Female choice tests show that gene flow is restricted among the completely plated and low plated morphs at both locations; behavioural isolation between these morphs is complete among Lake Azabachije fish, and nearly so (93% positive assortative mating) among White Sea basin fish. However, the experiments also demonstrate that there are no barriers to reproduction among the Azabachije and White Sea complete morphs, among the Azabachije low and White Sea complete morphs, nor among the Azabachije complete and White Sea low morphs. In addition, there is no evidence of barriers to gene flow among the low and partially plated morphs. Therefore, although gene flow is restricted among the extreme morphs within each locality, nevertheless gene exchange is possible, either directly or secondarily, among all phenotypes. The reproductive isolation between the complete and low morphs from the White Sea basin developed in situ no more than eight generations after the sticklebacks were introduced into an isolated freshwater pond. Therefore behavioural isolation can evolve very rapidly among the lateral plate phenotypes of Gasterosteus aculeatus.


Author(s):  
Linda Hagberg ◽  
Enrique Celemin ◽  
Iker Irisarri ◽  
Oliver Hawlitschek ◽  
J L Bella ◽  
...  

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.


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