scholarly journals The genomic and ecological context of hybridization affect the probability that symmetrical incompatibilities drive hybrid speciation

2017 ◽  
Author(s):  
Aaron A. Comeault

AbstractDespite examples of homoploid hybrid species, theoretical work describing when, where, and how we expect homoploid hybrid speciation to occur remains relatively rare. Here I explore the probability of homoploid hybrid speciation due to “symmetrical incompatibilities” under different selective and genetic scenarios. Through simulation, I test how genetic architecture and selection acting on traits that do not themselves generate incompatibilities interact to affect the probability that hybrids evolve symmetrical incompatibilities with their parent species. Unsurprisingly, selection against admixture at ‘adaptive’ loci that are linked to loci that generate incompatibilities tends to reduce the probability of evolving symmetrical incompatibilities. By contrast, selection that favors admixed genotypes at adaptive loci can promote the evolution of symmetrical incompatibilities. The magnitude of these outcomes is affected by the strength of selection, aspects of genetic architecture such as linkage relationships and the linear arrangement of loci along a chromosome, and the amount of hybridization following the formation of a hybrid zone. These results highlight how understanding the nature of selection, aspects of the genetics of traits affecting fitness, and the strength of reproductive isolation between hybridizing taxa can all be used to inform when we expect to observe homoploid hybrid speciation due to symmetrical incompatibilities.

2013 ◽  
Vol 59 (5) ◽  
pp. 667-674 ◽  
Author(s):  
Fabrice Eroukhmanoff ◽  
Richard I. Bailey ◽  
Glenn-Peter Sætre

Abstract Homoploid hybrid speciation (HHS) involves the recombination of two differentiated genomes into a novel, functional one without a change in chromosome number. Theoretically, there are numerous ways for two parental genomes to recombine. Hence, chance may play a large role in the formation of a hybrid species. If these genome combinations can evolve rapidly following hybridization and sympatric situations are numerous, recurrent homoploid hybrid speciation is a possibility. We argue that three different, but not mutually exclusive, types of contingencies could influence this process. First, many of these “hopeful monsters” of recombinant parent genotypes would likely have low fitness. Only specific combinations of parental genomic contributions may produce viable, intra-fertile hybrid species able to accommodate potential constraints arising from intragenomic conflict. Second, ecological conditions (competition, geography of the contact zones or the initial frequency of both parent species) might favor different outcomes ranging from sympatric coexistence to the formation of hybrid swarms and ultimately hybrid speciation. Finally, history may also play an important role in promoting or constraining recurrent HHS if multiple hybridization events occur sequentially and parental divergence or isolation differs along this continuum. We discuss under which conditions HHS may occur multiple times in parallel and to what extent recombination and selection may fuse the parent genomes in the same or different ways. We conclude by examining different approaches that might help to solve this intriguing evolutionary puzzle.


2018 ◽  
Vol 115 (39) ◽  
pp. 9761-9766 ◽  
Author(s):  
Aaron A. Comeault ◽  
Daniel R. Matute

Hybridization is often maladaptive and in some instances has led to the loss of biodiversity. However, hybridization can also promote speciation, such as during homoploid hybrid speciation, thereby generating biodiversity. Despite examples of homoploid hybrid species, the importance of hybridization as a speciation mechanism is still widely debated, and we lack a general understanding of the conditions most likely to generate homoploid hybrid species. Here we show that the level of genetic divergence between hybridizing species has a large effect on the probability that their hybrids evolve reproductive isolation. We find that populations of hybrids formed by parental species with intermediate levels of divergence were more likely to mate assortatively, and discriminate against their parental species, than those generated from weakly or strongly diverged parental species. Reproductive isolation was also found between hybrid populations, suggesting differential sorting of parental traits across populations. Finally, hybrid populations derived from three species were more likely to evolve reproductive isolation than those derived from two species, supporting arguments that hybridization-supplied genetic diversity can lead to the evolution of novel “adaptive systems” and promote speciation. Our results illustrate when we expect hybridization and admixture to promote hybrid speciation. Whether homoploid hybrid speciation is a common speciation mechanism in general remains an outstanding empirical question.


2015 ◽  
Author(s):  
Jean-Baptiste Leducq ◽  
Lou Nielly-Thibault ◽  
Guillaume Charron ◽  
Chris Eberlein ◽  
Jukka-Pekka Verta ◽  
...  

Hybridization is recognized as a powerful mechanism of speciation and a driving force in generating biodiversity. However, only few multicellular species, limited to a handful of plants and animals, have been shown to fulfill all the criteria of homoploid hybrid speciation. This lack of evidence could lead to the misconception that speciation by hybridization has a limited role in eukaryotes, particularly in single-celled organisms. Laboratory experiments have revealed that fungi such as budding yeasts can rapidly develop reproductive isolation and novel phenotypes through hybridization, showing that in principle homoploid speciation could occur in nature. Here we report a case of homoploid hybrid speciation in natural populations of the budding yeast Saccharomyces paradoxus inhabiting the North American forests. We show that the rapid evolution of chromosome architecture and an ecological context that led to secondary contact between nascent species drove the formation of an incipient hybrid species with a potentially unique ecological niche.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Guohong Albert Wu ◽  
Chikatoshi Sugimoto ◽  
Hideyasu Kinjo ◽  
Chika Azama ◽  
Fumimasa Mitsube ◽  
...  

AbstractThe origin and dispersal of cultivated and wild mandarin and related citrus are poorly understood. Here, comparative genome analysis of 69 new east Asian genomes and other mainland Asian citrus reveals a previously unrecognized wild sexual species native to the Ryukyu Islands: C. ryukyuensis sp. nov. The taxonomic complexity of east Asian mandarins then collapses to a satisfying simplicity, accounting for tachibana, shiikuwasha, and other traditional Ryukyuan mandarin types as homoploid hybrid species formed by combining C. ryukyuensis with various mainland mandarins. These hybrid species reproduce clonally by apomictic seed, a trait shared with oranges, grapefruits, lemons and many cultivated mandarins. We trace the origin of apomixis alleles in citrus to mangshanyeju wild mandarins, which played a central role in citrus domestication via adaptive wild introgression. Our results provide a coherent biogeographic framework for understanding the diversity and domestication of mandarin-type citrus through speciation, admixture, and rapid diffusion of apomictic reproduction.


2021 ◽  
Author(s):  
Homa Papoli Yazdi ◽  
Melissah Rowe ◽  
Mark Ravinet ◽  
Glenn-Peter Sætre ◽  
Caroline Øien Guldvog ◽  
...  

Hybridization is increasingly recognized as an important evolutionary force contributing novel variation for selection to act on. While mis-expression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa and contributes novel variation remains an open question, especially for hybrid species without an increase in ploidy. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an old homoploid hybrid, Italian sparrow, Passer italiae. Through comparing the gene expression of parental species and F1 hybrids to that of the Italian sparrow, we find evidence for strongly transgressive expression in the Italian sparrow, with 22% of the testis genes exhibiting expression patterns outside the range of both parent species, compared to only 0.37% in the F1s. In contrast, Italian sparrow ovary expression was similar to that of one parent species, the house sparrow (P. domesticus). Moreover, the Italian sparrow testis transcriptome is 26.2 -26.6 times as diverged from those of the parent species compared to how divergent their transcriptomes are in spite of it being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in energy production and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions have molded the hybrid transcriptome.


2014 ◽  
Vol 175 (3) ◽  
pp. 453-467 ◽  
Author(s):  
Giulia Mameli ◽  
Javier López-Alvarado ◽  
Emmanuele Farris ◽  
Alfonso Susanna ◽  
Rossella Filigheddu ◽  
...  

2019 ◽  
Author(s):  
Angélica Cuevas ◽  
Mark Ravinet ◽  
Glenn-Peter Sætre ◽  
Fabrice Eroukhmanoff

ABSTRACTHybridization increases genetic variation, hence hybrid species may have a strong evolutionary potential once their admixed genomes have stabilized and incompatibilities have been purged. Yet, little is known about how such hybrid lineages evolve at the genomic level following their formation, in particular the characteristics of their adaptive potential, i.e. constraints and facilitations of diversification. Here we investigate how the Italian sparrow (Passer italiae), a homoploid hybrid species, has evolved and locally adapted to its variable environment. Using restriction site-associated DNA sequencing (RAD-seq) on several populations across the Italian peninsula, we evaluate how genomic constraints and novel genetic variation have influenced population divergence and adaptation. We show that population divergence within this hybrid species has evolved in response to climatic variation. As in non-hybrid species, climatic differences may even reduce gene flow between populations, suggesting ongoing local adaptation. We report outlier genes associated with adaptation to climatic variation, known to be involved in beak morphology in other species. Most of the strongly divergent loci among Italian sparrow populations seem not to be differentiated between its parent species, the house and Spanish sparrow. Within the parental species, population divergence has occurred mostly in loci where different alleles segregate in the parent species, unlike in the hybrid, suggesting that novel combinations of parental alleles in the hybrid have not necessarily enhanced its evolutionary potential. Rather, our study suggests that constraints linked to incompatibilities may have restricted the evolution of this admixed genome, both during and after hybrid species formation.


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