Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

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.

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Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)

Frontiers in Plant Science ◽

10.3389/fpls.2020.573767 ◽

2021 ◽

Vol 11 ◽

Author(s):

Karolina Heyduk ◽

Edward V. McAssey ◽

Jane Grimwood ◽

Shengqiang Shu ◽

Jeremy Schmutz ◽

...

Keyword(s):

Parental Species ◽

Expression Patterns ◽

Hybrid Plant ◽

Sequencing Data ◽

Hybrid Species ◽

Chloroplast Genomes ◽

Important Trait ◽

Homoploid Hybrid ◽

Whole Genome Resequencing ◽

Expression Evidence

Hybridization in plants results in phenotypic and genotypic perturbations that can have dramatic effects on hybrid physiology, ecology, and overall fitness. Hybridization can also perturb epigenetic control of transposable elements, resulting in their proliferation. Understanding the mechanisms that maintain genomic integrity after hybridization is often confounded by changes in ploidy that occur in hybrid plant species. Homoploid hybrid species, which have no change in chromosome number relative to their parents, offer an opportunity to study the genomic consequences of hybridization in the absence of change in ploidy. Yucca gloriosa (Asparagaceae) is a young homoploid hybrid species, resulting from a cross between Yucca aloifolia and Yucca filamentosa. Previous analyses of ∼11 kb of the chloroplast genome and nuclear-encoded microsatellites implicated a single Y. aloifolia genotype as the maternal parent of Y. gloriosa. Using whole genome resequencing, we assembled chloroplast genomes from 41 accessions of all three species to re-assess the hybrid origins of Y. gloriosa. We further used re-sequencing data to annotate transposon abundance in the three species and mRNA-seq to analyze transcription of transposons. The chloroplast phylogeny and haplotype analysis suggest multiple hybridization events contributing to the origin of Y. gloriosa, with both parental species acting as the maternal donor. Transposon abundance at the superfamily level was significantly different between the three species; the hybrid was frequently intermediate to the parental species in TE superfamily abundance or appeared more similar to one or the other parent. In only one case—Copia LTR transposons—did Y. gloriosa have a significantly higher abundance relative to either parent. Expression patterns across the three species showed little increased transcriptional activity of transposons, suggesting that either no transposon release occurred in Y. gloriosa upon hybridization, or that any transposons that were activated via hybridization were rapidly silenced. The identification and quantification of transposon families paired with expression evidence paves the way for additional work seeking to link epigenetics with the important trait variation seen in this homoploid hybrid system.

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Genetic Architecture of Floral Traits in Iris hexagona and Iris fulva

Journal of Heredity ◽

10.1093/jhered/est059 ◽

2013 ◽

Vol 104 (6) ◽

pp. 853-861 ◽

Cited By ~ 11

Author(s):

Amanda N. Brothers ◽

Jessica G. Barb ◽

Evangeline S. Ballerini ◽

Douglas W. Drury ◽

Steven J. Knapp ◽

...

Keyword(s):

Genetic Architecture ◽

Floral Traits ◽

Iris Hexagona

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Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1809685115 ◽

2018 ◽

Vol 115 (39) ◽

pp. 9761-9766 ◽

Cited By ~ 13

Author(s):

Aaron A. Comeault ◽

Daniel R. Matute

Keyword(s):

Genetic Diversity ◽

Reproductive Isolation ◽

Genetic Divergence ◽

Adaptive Systems ◽

Parental Species ◽

Hybrid Speciation ◽

Hybrid Species ◽

Empirical Question ◽

Homoploid Hybrid

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.

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Hybridization and genome evolution I: The role of contingency during hybrid speciation

Current Zoology ◽

10.1093/czoolo/59.5.667 ◽

2013 ◽

Vol 59 (5) ◽

pp. 667-674 ◽

Cited By ~ 5

Author(s):

Fabrice Eroukhmanoff ◽

Richard I. Bailey ◽

Glenn-Peter Sætre

Keyword(s):

Chromosome Number ◽

Genome Evolution ◽

Hybrid Speciation ◽

Parent Species ◽

Large Role ◽

Hybrid Species ◽

Intragenomic Conflict ◽

Hybrid Swarms ◽

Homoploid Hybrid

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.

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The genomic organization of Ty3 /gypsy -like retrotransposons in Helianthus (Asteraceae) homoploid hybrid species

American Journal of Botany ◽

10.3732/ajb.0800337 ◽

2009 ◽

Vol 96 (9) ◽

pp. 1646-1655 ◽

Cited By ~ 29

Author(s):

S. Evan Staton ◽

Mark C. Ungerer ◽

Richard C. Moore

Keyword(s):

Genomic Organization ◽

Hybrid Species ◽

Homoploid Hybrid

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Enhanced drought-tolerance in the homoploid hybrid species Pinus densata: implication for its habitat divergence from two progenitors

New Phytologist ◽

10.1111/j.1469-8137.2009.03037.x ◽

2009 ◽

Vol 185 (1) ◽

pp. 204-216 ◽

Cited By ~ 35

Author(s):

Fei Ma ◽

Changming Zhao ◽

Richard Milne ◽

Mingfei Ji ◽

Litong Chen ◽

...

Keyword(s):

Drought Tolerance ◽

Hybrid Species ◽

Pinus Densata ◽

Homoploid Hybrid

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Speciation driven by hybridization and chromosomal plasticity in a wild yeast

10.1101/027383 ◽

2015 ◽

Author(s):

Jean-Baptiste Leducq ◽

Lou Nielly-Thibault ◽

Guillaume Charron ◽

Chris Eberlein ◽

Jukka-Pekka Verta ◽

...

Keyword(s):

Rapid Evolution ◽

Natural Populations ◽

Secondary Contact ◽

Hybrid Speciation ◽

Hybrid Species ◽

Chromosome Architecture ◽

The North ◽

Wild Yeast ◽

Homoploid Hybrid ◽

Powerful Mechanism

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.

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