THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION IN LOUISIANA IRISES: HYBRID FITNESS IN NATURE

Evolution ◽  
2009 ◽  
Vol 63 (10) ◽  
pp. 2581-2594 ◽  
Author(s):  
Sunni J. Taylor ◽  
Michael Arnold ◽  
Noland H. Martin
Keyword(s):  
Reproductive Isolation ◽  
Genetic Architecture ◽  
Hybrid Fitness

scholarly journals Ecological divergence in sympatry causes gene misregulation in hybrids

2019 ◽  
Author(s):  
Joseph A. McGirr ◽  
Christopher H. Martin
Keyword(s):  
Gene Expression ◽  
Reproductive Isolation ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Adaptive Divergence ◽  
Lower Hybrid ◽  
Hybrid Fitness ◽  
Hybrid Gene ◽  
San Salvador ◽  
Ecological Selection

AbstractEcological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. However, it is unknown whether divergent ecological selection on gene regulation can directly cause reproductive isolation. Selection favoring regulatory divergence between species could result in gene misregulation in F1 hybrids and ultimately lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to test this hypothesis in a young, sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, which consists of a dietary generalist and two novel trophic specialists – a molluscivore and a scale-eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misregulated in their F1 hybrids. Consistent with divergent ecological selection causing misregulation, a subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle, and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length – the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can cause hybrid gene misregulation which may act as a primary reproductive barrier between nascent species.SignificanceIt is unknown whether the same genes that regulate ecological traits can simultaneously contribute to reproductive barriers between species. We measured gene expression in two trophic specialist species of Cyprinodon pupfishes that rapidly diverged from a generalist ancestor. We found genes differentially expressed between species that also showed extreme expression levels in their hybrid offspring. Many of these genes showed signs of selection and have putative effects on the development of traits that are important for ecological specialization. This suggests that genetic variants contributing to adaptive trait divergence between parental species negatively interact to cause hybrid gene misregulation, potentially producing unfit hybrids. Such loci may be important barriers to gene flow during the early stages of speciation, even in sympatry.

scholarly journals Multi-locus interactions and the build-up of reproductive isolation

2020 ◽  
Vol 375 (1806) ◽  
pp. 20190543 ◽  
Author(s):  
I. Satokangas ◽  
S. H. Martin ◽  
H. Helanterä ◽  
J. Saramäki ◽  
J. Kulmuni
Keyword(s):  
Reproductive Isolation ◽  
Empirical Work ◽  
Hybrid Fitness ◽  
Epistatic Interactions ◽  
Genome Scans ◽  
Theoretical Approaches ◽  
Genome Wide ◽  
Experimental Approaches ◽  
Polymorphism Data

All genes interact with other genes, and their additive effects and epistatic interactions affect an organism's phenotype and fitness. Recent theoretical and empirical work has advanced our understanding of the role of multi-locus interactions in speciation. However, relating different models to one another and to empirical observations is challenging. This review focuses on multi-locus interactions that lead to reproductive isolation (RI) through reduced hybrid fitness. We first review theoretical approaches and show how recent work incorporating a mechanistic understanding of multi-locus interactions recapitulates earlier models, but also makes novel predictions concerning the build-up of RI. These include high variance in the build-up rate of RI among taxa, the emergence of strong incompatibilities producing localized barriers to introgression, and an effect of population size on the build-up of RI. We then review recent experimental approaches to detect multi-locus interactions underlying RI using genomic data. We argue that future studies would benefit from overlapping methods like ancestry disequilibrium scans, genome scans of differentiation and analyses of hybrid gene expression. Finally, we highlight a need for further overlap between theoretical and empirical work, and approaches that predict what kind of patterns multi-locus interactions resulting in incompatibilities will leave in genome-wide polymorphism data. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

scholarly journals Genomics of isolation in hybrids

2012 ◽  
Vol 367 (1587) ◽  
pp. 439-450 ◽  
Author(s):  
Zachariah Gompert ◽  
Thomas L. Parchman ◽  
C. Alex Buerkle
Keyword(s):  
Reproductive Isolation ◽  
Genetic Architecture ◽  
Large Scale ◽  
Empirical Studies ◽  
Hybrid Zones ◽  
Direct Measure ◽  
Fitness Effects ◽  
Outlier Loci ◽  
Admixed Population ◽  
Genome Level

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.

scholarly journals Cytonuclear Genetic Incompatibilities in Plant Speciation

Plants ◽  
2020 ◽  
Vol 9 (4) ◽  
pp. 487 ◽  
Author(s):  
Zoé Postel ◽  
Pascal Touzet
Keyword(s):  
Reproductive Isolation ◽  
Plant Species ◽  
Mating Systems ◽  
Cell Function ◽  
Evolutionary Processes ◽  
Hybrid Fitness ◽  
Plant Mating Systems ◽  
The Impact ◽  
Cytonuclear Interaction ◽  
Endosymbiotic Origin

Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.

scholarly journals Limited intrinsic postzygotic reproductive isolation despite chromosomal rearrangements between closely related sympatric species of small ermine moths (Lepidoptera: Yponomeutidae)

2019 ◽  
Vol 128 (1) ◽  
pp. 44-58 ◽  
Author(s):  
Katerina H Hora ◽  
František Marec ◽  
Peter Roessingh ◽  
Steph B J Menken
Keyword(s):  
Reproductive Isolation ◽  
Parental Species ◽  
Meiotic Chromosome ◽  
Chromosomal Rearrangements ◽  
Sympatric Species ◽  
Hybrid Fitness ◽  
New Host ◽  
Closely Related Species ◽  
Postzygotic Reproductive Isolation

Abstract In evolutionarily young species and sympatric host races of phytophagous insects, postzygotic incompatibility is often not yet fully developed, but reduced fitness of hybrids is thought to facilitate further divergence. However, empirical evidence supporting this hypothesis is limited. To assess the role of reduced hybrid fitness, we studied meiosis and fertility in hybrids of two closely related small ermine moths, Yponomeuta padella and Yponomeuta cagnagella, and determined the extent of intrinsic postzygotic reproductive isolation. We found extensive rearrangements between the karyotypes of the two species and irregularities in meiotic chromosome pairing in their hybrids. The fertility of reciprocal F1 and, surprisingly, also of backcrosses with both parental species was not significantly decreased compared with intraspecific offspring. The results indicate that intrinsic postzygotic reproductive isolation between these closely related species is limited. We conclude that the observed chromosomal rearrangements are probably not the result of an accumulation of postzygotic incompatibilities preventing hybridization. Alternative explanations, such as adaptation to new host plants, are discussed.

scholarly journals The Genetic Architecture of Reproductive Isolation in Louisiana Irises: Flowering Phenology

Genetics ◽  
2007 ◽  
Vol 175 (4) ◽  
pp. 1803-1812 ◽  
Author(s):  
Noland H. Martin ◽  
Amy C. Bouck ◽  
Michael L. Arnold
Keyword(s):  
Reproductive Isolation ◽  
Genetic Architecture ◽  
Flowering Phenology

scholarly journals Population genomic evidence of selection on structural variants in a natural hybrid zone

2022 ◽  
Author(s):  
Linyi Zhang ◽  
Samridhi Chaturvedi ◽  
Chris Nice ◽  
Lauren Lucas ◽  
Zachariah Gompert
Keyword(s):  
Reproductive Isolation ◽  
Hybrid Zone ◽  
Structural Variants ◽  
Hybrid Fitness ◽  
Genome Wide ◽  
Oxford Nanopore ◽  
Jackson Hole ◽  
Long Read ◽  
Genomic Regions

Structural variants (SVs) can promote speciation by directly causing reproductive isolation or by suppressing recombination across large genomic regions. Whereas examples of each mechanism have been documented, systematic tests of the role of SVs in speciation are lacking. Here, we take advantage of long-read (Oxford nanopore) whole-genome sequencing and a hybrid zone between two Lycaeides butterfly taxa (L. melissa and Jackson Hole Lycaeides) to comprehensively evaluate genome-wide patterns of introgression for SVs and relate these patterns to hypotheses about speciation. We found >100,000 SVs segregating within or between the two hybridizing species. SVs and SNPs exhibited similar levels of genetic differentiation between species, with the exception of inversions, which were more differentiated. We detected credible variation in patterns of introgression among SV loci in the hybrid zone, with 562 of 1419 ancestry-informative SVs exhibiting genomic clines that deviating from null expectations based on genome-average ancestry. Overall, hybrids exhibited a directional shift towards Jackson Hole Lycaeides ancestry at SV loci, consistent with the hypothesis that these loci experienced more selection on average then SNP loci. Surprisingly, we found that deletions, rather than inversions, showed the highest skew towards excess introgression from Jackson Hole Lycaeides. Excess Jackson Hole Lycaeides ancestry in hybrids was also especially pronounced for Z-linked SVs and inversions containing many genes. In conclusion, our results show that SVs are ubiquitous and suggest that SVs in general, but especially deletions, might contribute disproportionately to hybrid fitness and thus (partial) reproductive isolation.

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