scholarly journals In search of the Goldilocks zone for hybrid speciation

2018 ◽  
Author(s):  
Alexandre Blanckaert ◽  
Claudia Bank

AbstractHybridization has recently gained considerable interest both as a unique window for observing speciation mechanisms and as a potential engine of speciation. The latter remains a controversial topic. It was recently hypothesized that the reciprocal sorting of genetic incompatibilities from parental species could result in hybrid speciation, when the hybrid population maintains a mixed combination of the parental incompatibilities that prevents further gene exchange with both parental populations. However, the specifics of the purging/sorting process of multiple incompatibilities have not been examined theoretically.We here investigate the allele-frequency dynamics of an isolated hybrid population that results from a single hybridization event. Using models of 2 or 4 loci, we investigate the fate of one or two genetic incompatibilities of the Dobzhansky-Muller type (DMIs). We study how various parameters affect both the sorting/purging of the DMIs and the probability of observing hybrid speciation by reciprocal sorting. We find that the probability of hybrid speciation is strongly dependent on the linkage architecture (i.e. the order and recombination distance between loci along chromosomes), the population size of the hybrid population, and the initial relative contribution of the parental populations to the hybrid population. We identify a Goldilocks zone for specific linkage architectures and intermediate recombination rates, in which hybrid speciation becomes highly probable. Whereas an equal contribution of parental populations to the hybrid populations maximizes the hybrid speciation probability in the Goldilocks zone, other linkage architectures yield unintuitive asymmetric maxima. We provide an explanation for this pattern, and discuss our results both with respect to the best conditions for observing hybrid speciation in nature and their implications regarding patterns of introgression in hybrid zones.SummaryHybridization is observed ubiquitously in nature. Its outcome can range from extinction to the creation of new species. With respect to the latter, the probability of homoploid hybrid speciation, i.e. the formation of a new species as a result of an hybridization event without changes in the ploidy of the organism, is a hotly debated topic. Here, we analyze a minimal model for homoploid hybrid speciation, in which reproductive isolation is achieved by means of (postzygotic) Dobzhansky-Muller incompatibilities. When these postzygotic genetic incompatibilities are resolved in the hybrid population, their reciprocal sorting can result in reproductive isolation from both parental populations, thus creating a hybrid species. We show that, in accordance with the current literature, hybrid speciation tends to be rare. However, specific arrangements of the genes responsible for reproductive isolation can make reciprocal sorting almost unavoidable and thus create barriers to the parental population in an almost deterministic matter. We discuss the implications of these results for hybrid speciation and patterns of introgression in nature.

2015 ◽  
Vol 282 (1807) ◽  
pp. 20150157 ◽  
Author(s):  
Vladimir A. Lukhtanov ◽  
Nazar A. Shapoval ◽  
Boris A. Anokhin ◽  
Alsu F. Saifitdinova ◽  
Valentina G. Kuznetsova

Genomes of numerous diploid plant and animal species possess traces of interspecific crosses, and many researches consider them as support for homoploid hybrid speciation (HHS), a process by which a new reproductively isolated species arises through hybridization and combination of parts of the parental genomes, but without an increase in ploidy. However, convincing evidence for a creative role of hybridization in the origin of reproductive isolation between hybrid and parental forms is extremely limited. Here, through studying Agrodiaetus butterflies, we provide proof of a previously unknown mode of HHS based on the formation of post-zygotic reproductive isolation via hybridization of chromosomally divergent parental species and subsequent fixation of a novel combination of chromosome fusions/fissions in hybrid descendants. We show that meiotic segregation, operating in the hybrid lineage, resulted in the formation of a new diploid genome, drastically rearranged in terms of chromosome number. We also demonstrate that during the heterozygous stage of the hybrid species formation, recombination was limited between rearranged chromosomes of different parental origin, representing evidence that the reproductive isolation was a direct consequence of hybridization.


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.


2019 ◽  
Author(s):  
Elizabeth S.C. Scordato ◽  
Chris C.R. Smith ◽  
Georgy A. Semenov ◽  
Yu Liu ◽  
Matthew R. Wilkins ◽  
...  

AbstractMigratory divides are proposed to be catalysts for speciation across a diversity of taxa. However, the relative contribution of migratory behavior to reproductive isolation is difficult to test. Comparing reproductive isolation in hybrid zones with and without migratory divides offers a rare opportunity to directly examine the contribution of divergent migratory behavior to reproductive barriers. We show that across replicate sampling transects of two pairs of barn swallow (Hirundo rustica) subspecies, strong reproductive isolation coincided with an apparent migratory divide spanning 20 degrees of latitude. A third subspecies pair exhibited no evidence for a migratory divide and hybridized extensively. Within migratory divides, migratory phenotype was associated with assortative mating, implicating a central contribution of divergent migratory behavior to reproductive barriers. The remarkable geographic coincidence between migratory divides and genetic breaks supports a longstanding hypothesis that the Tibetan Plateau is a substantial barrier contributing to the diversity of Siberian avifauna.


Science ◽  
2017 ◽  
Vol 359 (6372) ◽  
pp. 224-228 ◽  
Author(s):  
Sangeet Lamichhaney ◽  
Fan Han ◽  
Matthew T. Webster ◽  
Leif Andersson ◽  
B. Rosemary Grant ◽  
...  

Homoploid hybrid speciation in animals has been inferred frequently from patterns of variation, but few examples have withstood critical scrutiny. Here we report a directly documented example, from its origin to reproductive isolation. An immigrant Darwin’s finch to Daphne Major in the Galápagos archipelago initiated a new genetic lineage by breeding with a resident finch (Geospiza fortis). Genome sequencing of the immigrant identified it as aG. conirostrismale that originated on Española >100 kilometers from Daphne Major. From the second generation onward, the lineage bred endogamously and, despite intense inbreeding, was ecologically successful and showed transgressive segregation of bill morphology. This example shows that reproductive isolation, which typically develops over hundreds of generations, can be established in only three.


2018 ◽  
Vol 285 (1874) ◽  
pp. 20172081 ◽  
Author(s):  
Paola Pulido-Santacruz ◽  
Alexandre Aleixo ◽  
Jason T. Weir

We possess limited understanding of how speciation unfolds in the most species-rich region of the planet—the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.


Zootaxa ◽  
2021 ◽  
Vol 4910 (1) ◽  
pp. 1-92
Author(s):  
JEFFREY A. COLE ◽  
DAVID B. WEISSMAN ◽  
DAVID C. LIGHTFOOT ◽  
NORIHIRO UESHIMA ◽  
ELŻBIETA WARCHAŁOWSKA-ŚLIWA ◽  
...  

The Nearctic shield-back katydid genus Neduba is revised. Species boundaries were demarcated by molecular phylogenetic analysis, morphology, quantitative analysis of calling songs, and karyotypes. Nine previously described species are redescribed: N. carinata, N. castanea, N. convexa, N. diabolica, N. extincta, N. macneilli, N. propsti, N. sierranus, and N. steindachneri, and twelve new species are described: N. ambagiosa sp. n., N. arborea sp. n., N. cascadia sp. n., N. duplocantans sp. n., N. inversa sp. n., N. longiplutea sp. n., N. lucubrata sp. n., N. oblongata sp. n., N. prorocantans sp. n., N. radicata sp. n., N. radocantans sp. n., and N. sequoia sp. n. We chose a lectotype for N. steindachneri and transferred N. picturata from a junior synonym of N. diabolica to a junior synonym of N. steindachneri. Diversification in this relict group reflects cycles of allopatric isolation and secondary contact amidst the tumultuous, evolving geography of western North America. The taxonomy and phylogenies presented in this revision lay the groundwork for studies of speciation, biogeography, hybrid zones, and behavioral evolution. Given that one Neduba species is already extinct from human environmental disturbance, we suggest conservation priorities for the genus. 


Genetics ◽  
2019 ◽  
Vol 211 (3) ◽  
pp. 1059-1073 ◽  
Author(s):  
Mark S. Hibbins ◽  
Matthew W. Hahn

Introgression is a pervasive biological process, and many statistical methods have been developed to infer its presence from genomic data. However, many of the consequences and genomic signatures of introgression remain unexplored from a methodological standpoint. Here, we develop a model for the timing and direction of introgression based on the multispecies network coalescent, and from it suggest new approaches for testing introgression hypotheses. We suggest two new statistics, D1 and D2, which can be used in conjunction with other information to test hypotheses relating to the timing and direction of introgression, respectively. D1 may find use in evaluating cases of homoploid hybrid speciation (HHS), while D2 provides a four-taxon test for polarizing introgression. Although analytical expectations for our statistics require a number of assumptions to be met, we show how simulations can be used to test hypotheses about introgression when these assumptions are violated. We apply the D1 statistic to genomic data from the wild yeast Saccharomyces paradoxus—a proposed example of HHS—demonstrating its use as a test of this model. These methods provide new and powerful ways to address questions relating to the timing and direction of introgression.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190544 ◽  
Author(s):  
Huiying Shang ◽  
Jaqueline Hess ◽  
Melinda Pickup ◽  
David L. Field ◽  
Pär K. Ingvarsson ◽  
...  

Many recent studies have addressed the mechanisms operating during the early stages of speciation, but surprisingly few studies have tested theoretical predictions on the evolution of strong reproductive isolation (RI). To help address this gap, we first undertook a quantitative review of the hybrid zone literature for flowering plants in relation to reproductive barriers. Then, using Populus as an exemplary model group, we analysed genome-wide variation for phylogenetic tree topologies in both early- and late-stage speciation taxa to determine how these patterns may be related to the genomic architecture of RI. Our plant literature survey revealed variation in barrier complexity and an association between barrier number and introgressive gene flow. Focusing on Populus, our genome-wide analysis of tree topologies in speciating poplar taxa points to unusually complex genomic architectures of RI, consistent with earlier genome-wide association studies. These architectures appear to facilitate the ‘escape’ of introgressed genome segments from polygenic barriers even with strong RI, thus affecting their relationships with recombination rates. Placed within the context of the broader literature, our data illustrate how phylogenomic approaches hold great promise for addressing the evolution and temporary breakdown of RI during late stages of speciation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.


2016 ◽  
Vol 103 (2) ◽  
pp. 246-259 ◽  
Author(s):  
J. R. P. Worth ◽  
M. J. Larcombe ◽  
S. Sakaguchi ◽  
J. R. Marthick ◽  
D. M. J. S. Bowman ◽  
...  

2012 ◽  
Vol 367 (1587) ◽  
pp. 439-450 ◽  
Author(s):  
Zachariah Gompert ◽  
Thomas L. Parchman ◽  
C. Alex Buerkle

Hybrid zones are common in nature and can offer critical insights into the dynamics and components of reproductive isolation. Hybrids between diverged lineages are particularly informative about the genetic architecture of reproductive isolation, because introgression in an admixed population is a direct measure of isolation. In this paper, we combine simulations and a new statistical model to determine the extent to which different genetic architectures of isolation leave different signatures on genome-level patterns of introgression. We found that reproductive isolation caused by one or several loci of large effect caused greater heterogeneity in patterns of introgression than architectures involving many loci with small fitness effects, particularly when isolating factors were closely linked. The same conditions that led to heterogeneous introgression often resulted in a reasonable correspondence between outlier loci and the genetic loci that contributed to isolation. However, demographic conditions affected both of these results, highlighting potential limitations to the study of the speciation genomics. Further progress in understanding the genomics of speciation will require large-scale empirical studies of introgression in hybrid zones and model-based analyses, as well as more comprehensive modelling of the expected levels of isolation with different demographies and genetic architectures of isolation.


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