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.2023 Jan;130(1):40-52.
doi: 10.1038/s41437-022-00576-4. Epub 2022 Dec 9.

Rapid evolution of hybrid breakdown following recent divergence with gene flow in Senecio species on Mount Etna, Sicily

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Rapid evolution of hybrid breakdown following recent divergence with gene flow in Senecio species on Mount Etna, Sicily

Edgar L Y Wong et al. Heredity (Edinb).2023 Jan.

Abstract

How do nascent species evolve reproductive isolation during speciation with on-going gene flow? How do hybrid lineages become stabilised hybrid species? While commonly used genomic approaches provide an indirect way to identify species incompatibility factors, synthetic hybrids generated from interspecific crosses allow direct pinpointing of phenotypic traits involved in incompatibilities and the traits that are potentially adaptive in hybrid species. Here we report the analysis of phenotypic variation and hybrid breakdown in crosses between closely-related Senecio aethnensis and S. chrysanthemifolius, and their homoploid hybrid species, S. squalidus. The two former species represent a likely case of recent (<200 ky) speciation with gene flow driven by adaptation to contrasting conditions of high- and low-elevations on Mount Etna, Sicily. As these species form viable and fertile hybrids, it remains unclear whether they have started to evolve reproductive incompatibility. Our analysis represents the first study of phenotypic variation and hybrid breakdown involving multiple Senecio hybrid families. It revealed wide range of variation in multiple traits, including the traits previously unrecorded in synthetic hybrids. Leaf shape, highly distinct between S. aethnensis and S. chrysanthemifolius, was extremely variable in F2 hybrids, but more consistent in S. squalidus. Our study demonstrates that interspecific incompatibilities can evolve rapidly despite on-going gene flow between the species. Further work is necessary to understand the genetic bases of these incompatibilities and their role in speciation with gene flow.

© 2022. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Crossing design in this study.
F0 parents in 193B, B228, and the derived lines of a reciprocal cross (B71 and B87) were grown from seeds collected from different populations.
Fig. 2
Fig. 2. Photos showing trait variabilities and potential signs of hybrid breakdown.
a Leaf shape variation in the same F2 family;b A F2 plant showing early mortality;c Left: leaf without trichomes (parental phenotype); right: F2 with trichomes;d F2 capitula that lack ray florets.
Fig. 3
Fig. 3. Box plots of each leaf phenotypic trait quantified in wildS. squalidus, F2 individuals, greenhouse-grown and wild ExeterS. squalidus samples respectively.
* indicates significance of each pairwise Kruskal-Wallis test (*:P-value < 0.05; **:P-value < 0.005; ***:P-value < 0.0005; n.s. = not significant).
Fig. 4
Fig. 4. Ordination plots of F2 individuals and all wildS. squalidus samples.
a PCA. Ellipses represent 95% CI of the data;b NMDS plot. Polygon encloses all data points. Loading values for PC1 and PC2 are embedded in plot (a). Full tables of loading values are in Supplementary Table 5.
Fig. 5
Fig. 5. Ordination plots of (1) F2 individuals, the hybrid speciesS. squalidus Exeter population that were (2) collected from the field and (3) grown from wild cuttings in the greenhouse.
a PCA. Ellipses represent 95% CI of the data;b NMDS plot. Polygon encloses all data points. Loading values for PC1 and PC2 are embedded in plot (a). Full tables of loading values are in Supplementary Table 5.
Fig. 6
Fig. 6. Ordination plot (PCA) of the four F2 families.
Ellipses represent 95% CI of the data. Loading values for PC1 and PC2 are embedded in the plots. Full tables of loading values are in Supplementary Table 5.
Fig. 7
Fig. 7. Box plots of each phenotypic trait quantified in the four F2 families.
P-values for Kruskal-Wallis test are indicated at the top of each plot; letters above each box represent groupings following results of Wilcoxon rank-sum test. Detailed results of the two tests can be found in the supplementary tables.
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