Selection against recombinant hybrids maintains reproductive isolation in hybridizing <i>Populus</i> species despite F<sub>1</sub> fertility and recurrent gene flow

Christe, Camille; Stölting, Kai N.; Bresadola, Luisa; Fussi, Barbara; Heinze, Berthold; Wegmann, Daniel; Lexer, Christian

doi:10.1111/mec.13587

Cited by 88 publications

(147 citation statements)

References 97 publications

(286 reference statements)

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“…Consistent with the results of a recent study from the European hybrid zones32, our current analysis also found that F1 hybrids prevailed in the Irtysh River hybrid zone; however, due to differences in analytical methods, the hybrid P. × canescens had previously been considered to be highly recombinant252728. Their prevalence in both of these geographically distant hybrid zones are unlikely to be strongly affected by stochastic or locality-specific events, but rather reflect the high fitness of such genomic patterns of hybrids due to heterosis283132.…”

Section: Discussionsupporting

confidence: 92%

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Zeng

Zhang

Duan

et al. 2016

Sci Rep

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In plants, the maintenance of species integrity despite hybridization has often been explained by the co-adaption of nuclear gene complexes. However, the interaction between plastid and nuclear sub-genomes has been underestimated. Here, we analyzed the genetic structure of a Populus alba and P. tremula hybrid zone along the Irtysh River system in the Altai region, northwest China, using both nuclear microsatellites and plastid DNA sequences. We found high interspecific differentiation, although the hybrid P. × canescens was prevalent. Bayesian inference classified most hybrids into F1, followed by a few back-crosses to P. alba, and fewer F2 hybrids and back-crosses to P. tremula, indicating a few introgressions but preference toward P. alba. When plastid haplotypes in parental species were distinct, P. × canescens carried the haplotypes of both parents, but showed significant linkage between intraspecific haplotype and nuclear genotypes at several microsatellite loci. Selection, rather than migration and assortative mating, might have contributed to such plastid-nuclear disequilibria. By removing later-generated hybrids carrying interspecific combinations of haplotype and nuclear genotypes, plastid-nuclear incompatibility has greatly limited the gene exchange between P. alba and P. tremula via backcrossing with hybrids, demonstrating a significant association between plastid haplotype and the proportion of nuclear admixture.

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Section: Discussionsupporting

confidence: 92%

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Zeng

Zhang

Duan

et al. 2016

Sci Rep

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“…(2016) corresponds to

{\overset{β}{true}}_{0} = 2.963

{\overset{β}{true}}_{1} = 2.777

and

{\overset{β}{true}}_{2} = 0.934

, which supports the predictions of directional selection toward higher heterozygosity, and near‐symmetrical diversifying selection on the hybrid index.…”

Section: Models and Resultssupporting

confidence: 75%

“…2012, 2014; Christe et al. 2016). These authors scored survival over four years in a common‐garden environment, and fit a generalized linear model to their binary data (binary logistic regression, with “family” as a random effect), and predictors including linear and quadratic terms in p 12 and h .…”

Section: Models and Resultsmentioning

confidence: 99%

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Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

2018

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Natural selection plays a variety of roles in hybridization, speciation, and admixture. Most research has focused on two extreme cases: crosses between closely related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. But many natural populations must fall into intermediate regimes, with multiple types of gene interaction, and these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, which were designed for the extreme cases, and invoke either mildly deleterious recessives, or discrete hybrid incompatibilities. Our model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants (Zea, Populus, and Senecio) and animals (Mus, Teleogryllus, and Drosophila). The predictions are generally supported, and the model explains a number of surprising empirical patterns. Our approach enables novel and complementary uses of genome‐wide datasets, which do not depend on identifying outlier loci, or “speciation genes” with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

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“…As shown in Christe et al (2016), chromosomes of perfect F1 individuals of an interspecific hybrid are (almost) completely of heterospecific ancestry. Sequence data of the parents of INRA 717-1B4 would therefore be very helpful to fulfil this task and to resolve the two haplotypes; however, unfortunately, the parents of INRA 717-1B4 are not available anymore.…”

Section: Discussionmentioning

confidence: 99%

Whole-genome draft assembly of Populus tremula x P. alba clone INRA 717-1B4

Mäder¹,

Paslier

Bounon

et al. 2016

Silvae Genetica

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Populus trichocarpa and P. deltoides are the only Populus species known to date to have a publicly available nuclear genome sequence that has been assembled to chromosomes and annotated (https://phytozome.jgi.doe.gov/). Here we focus on the clone INRA 717-1B4, a female P. tremula x P. alba (P. x canescens) interspecific hybrid that is universally used by scientists worldwide as a tree model in transgenic experiments. The already available INRA 717-1B4 nuclear genomic resource (v1.1 of sPta717 at http://aspendb.uga.edu/index.php/databases/ spta-717-genome) presents only INRA 717-1B4 genomic regions with high similarity to the P. trichocarpa genomic reference sequences. We assembled draft genomic scaffolds by a combination of de novo assembly with reference-based assembly using 30x resequencing NGS data (Illumina MiSeq® and Ion Torrent Ion PGM™) of INRA 717-1B4. In total, 419,969 scaffolds of length larger than 500 bp were generated. The mean length of the scaffolds is 2,166 bp and the size of the largest scaffold 84,573 bp. The N50 contig length is 3,850 bp when considering contigs larger than 1,000 bp. Probably due to the high level of heterozygosity of this interspecific hybrid, the accumulated scaffold length is with 0.9 GB about twice the expected size of the haploid nuclear genome. DNA sequences of the genomic scaffolds of INRA 717-1B4 are publicly available for Blast analyses and download via the new INRA web portal at https://urgi. versailles.inra.fr/Species/Forest-trees/Populus/Clone-INRA-717-1B4/. This new genomic sequence resource will complement the already available INRA 717-1B4 resources and will facilitate the future optimization of genetic transformation experiments to discover gene function.

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Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F₁ fertility and recurrent gene flow

Cited by 88 publications

References 97 publications

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

Whole-genome draft assembly of Populus tremula x P. alba clone INRA 717-1B4

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Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F1 fertility and recurrent gene flow

Cited by 88 publications

References 97 publications

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Genetic structure of Populus hybrid zone along the Irtysh River provides insight into plastid-nuclear incompatibility

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

Whole-genome draft assembly of Populus tremula x P. alba clone INRA 717-1B4

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Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F₁ fertility and recurrent gene flow