scholarly journals Mass of genes rather than master genes underlie the genomic architecture of amphibian speciation

2021 ◽  
Vol 118 (36) ◽  
pp. e2103963118
Author(s):  
Christophe Dufresnes ◽  
Alan Brelsford ◽  
Daniel L. Jeffries ◽  
Glib Mazepa ◽  
Tomasz Suchan ◽  
...  

The genetic architecture of speciation, i.e., how intrinsic genomic incompatibilities promote reproductive isolation (RI) between diverging lineages, is one of the best-kept secrets of evolution. To directly assess whether incompatibilities arise in a limited set of large-effect speciation genes, or in a multitude of loci, we examined the geographic and genomic landscapes of introgression across the hybrid zones of 41 pairs of frog and toad lineages in the Western Palearctic region. As the divergence between lineages increases, phylogeographic transitions progressively become narrower, and larger parts of the genome resist introgression. This suggests that anuran speciation proceeds through a gradual accumulation of multiple barrier loci scattered across the genome, which ultimately deplete hybrid fitness by intrinsic postzygotic isolation, with behavioral isolation being achieved only at later stages. Moreover, these loci were disproportionately sex linked in one group (Hyla) but not in others (Rana and Bufotes), implying that large X-effects are not necessarily a rule of speciation with undifferentiated sex chromosomes. The highly polygenic nature of RI and the lack of hemizygous X/Z chromosomes could explain why the speciation clock ticks slower in amphibians compared to other vertebrates. The clock-like dynamics of speciation combined with the analytical focus on hybrid zones offer perspectives for more standardized practices of species delimitation.

2019 ◽  
Author(s):  
Darren E. Irwin

AbstractAssortative mating and other forms of partial prezygotic isolation are often viewed as being more important than partial postzygotic isolation (low fitness of hybrids) early in the process of speciation. Here I simulate secondary contact between two populations (‘species’) to examine effects of pre- and postzygotic isolation in preventing blending. A small reduction in hybrid fitness (e.g., 10%) produces a narrower hybrid zone than a strong but imperfect mating preference (e.g., 10x stronger preference for conspecific over heterospecific mates). This is because, in the latter case, rare F1 hybrids find each other attractive (due to assortative mating), leading to the gradual buildup of a full continuum of intermediates between the two species. The cline is narrower than would result from purely neutral diffusion over the same number of generations, largely due to the frequency-dependent mating disadvantage of individuals of rare mating types. Hybrids tend to pay this cost of rarity more than pure individuals, meaning there is an induced postzygotic isolation effect of assortative mating. These results prompt a questioning of the concept of partial prezygotic isolation, since it is not very isolating unless there is also postzygotic isolation.


2019 ◽  
Vol 37 (3) ◽  
pp. 711-729 ◽  
Author(s):  
Rachel L Moran ◽  
Julian M Catchen ◽  
Rebecca C Fuller

Abstract Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.


Genetics ◽  
1999 ◽  
Vol 152 (2) ◽  
pp. 713-727 ◽  
Author(s):  
Loren H Rieseberg ◽  
Jeannette Whitton ◽  
Keith Gardner

Abstract Genetic analyses of reproductive barriers represent one of the few methods by which theories of speciation can be tested. However, genetic study is often restricted to model organisms that have short generation times and are easily propagated in the laboratory. Replicate hybrid zones with a diversity of recombinant genotypes of varying age offer increased resolution for genetic mapping experiments and expand the pool of organisms amenable to genetic study. Using 88 markers distributed across 17 chromosomes, we analyze the introgression of chromosomal segments of Helianthus petiolaris into H. annuus in three natural hybrid zones. Introgression was significantly reduced relative to neutral expectations for 26 chromosomal segments, suggesting that each segment contains one or more factors that contribute to isolation. Pollen sterility is significantly associated with 16 of these 26 segments, providing a straightforward explanation of why this subset of blocks is disadvantageous in hybrids. In addition, comparison of rates of introgression across colinear vs. rearranged chromosomes indicates that close to 50% of the barrier to introgression is due to chromosomal rearrangements. These results demonstrate the utility of hybrid zones for identifying factors contributing to isolation and verify the prediction of increased resolution relative to controlled crosses.


2017 ◽  
Author(s):  
Thomas Blankers ◽  
Kevin P. Oh ◽  
Aureliano Bombarely ◽  
Kerry L. Shaw

ABSTRACTPhenotypic evolution and speciation depend on recombination in many ways. Within populations, recombination can promote adaptation by bringing together favorable mutations and decoupling beneficial and deleterious alleles. As populations diverge, cross-over can give rise to maladapted recombinants and impede or reverse diversification. Suppressed recombination due to genomic rearrangements, modifier alleles, and intrinsic chromosomal properties may offer a shield against maladaptive gene flow eroding co-adapted gene complexes. Both theoretical and empirical results support this relationship. However, little is known about this relationship in the context of behavioral isolation, where co-evolving signals and preferences are the major hybridization barrier. Here we examine the genomic architecture of recently diverged, sexually isolated Hawaiian swordtail crickets (Laupala). We assemble a de novo genome and generate three dense linkage maps from interspecies crosses. In line with expectations based on the species’ recent divergence and successful interbreeding in the lab, the linkage maps are highly collinear and show no evidence for large-scale chromosomal rearrangements. The maps were then used to anchor the assembly to pseudomolecules and estimate recombination rates across the genome. We tested the hypothesis that loci involved in behavioral isolation (song and preference divergence) are in regions of low interspecific recombination. Contrary to our expectations, a genomic region where a male song QTL co-localizes with a female preference QTL was not associated with particularly low recombination rates. This study provides important novel genomic resources for an emerging evolutionary genetics model system and suggests that trait-preference co-evolution is not necessarily facilitated by locally suppressed recombination.


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.


2021 ◽  
pp. 1-12
Author(s):  
Daniel Jablonski ◽  
Neftalí Sillero ◽  
Oleksandra Oskyrko ◽  
Adriana Bellati ◽  
Andris Čeirāns ◽  
...  

Abstract The slow-worm lizards (Anguis) comprise five species occurring throughout most of the Western Palearctic. Although these species are relatively uniform morphologically – with the exception of A. cephallonica, which exhibits a quite unique morphology – they are genetically deeply divergent. Here, we provide detailed distribution maps for each species and discuss their biogeography and conservation based on updated genetic data and a robust distribution database. We pay particular attention to the so called ‘grey zone’, which typically represents secondary contact zones and in some cases confirmed or presumed hybrid zones. Four of the five species live in parapatry, while only two species, A. cephallonica and A. graeca from the southern Balkans occur in partial sympatry. Further research should focus on the eco-evolutionary interactions between species in contact, including their hybridization rates, to reveal deeper details of the slow-worm evolutionary and natural history.


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.


Evolution ◽  
2009 ◽  
Vol 63 (10) ◽  
pp. 2581-2594 ◽  
Author(s):  
Sunni J. Taylor ◽  
Michael Arnold ◽  
Noland H. Martin

1993 ◽  
Vol 71 (2) ◽  
pp. 233-237 ◽  
Author(s):  
Marta Martínez Wells

Courtship songs are an important reproductive barrier in lacewings of the genus Chrysoperla, so heterotypic matings should occur less readily than homotypic matings. In addition, if song morphs have become separate species, there may be some postzygotic isolation between song morphs. Two generations of crosses using sympatric P1 and P3 morphs of Chrysoperla plorabunda provide evidence for both hypotheses. In the first stage of the experiment, egg laying (an indication of mating success) was delayed by a week in heterotypic crosses compared with homotypic crosses, and hatching success of eggs from hybrid crosses was 16% lower than that from control crosses. In the second stage of the experiment, backcrosses involving P3 morph males or females were the least successful in mating. When pairs did mate, they did so a week later than in the other crosses. Thus, behavioral isolation delays heterotypic matings when females are not given a choice of mates. These results provide some genetic evidence that the song morphs of the C. plorabunda complex are biological species.


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