An evaluation of alternative explanations for widespread cytonuclear discordance in annual sunflowers (Helianthus)

Abstract

Cytonuclear discordance is commonly observed in phylogenetic studies, yet few studies have tested whether these patterns reflect incomplete lineage sorting or organellar introgression. Here, we used whole-chloroplast sequence data in combination with over 1000 nuclear single-nucleotide polymorphisms to clarify the extent of cytonuclear discordance in wild annual sunflowers (Helianthus), and to test alternative explanations for such discordance. Our phylogenetic analyses indicate that cytonuclear discordance is widespread within this group, both in terms of the relationships among species and among individuals within species. Simulations of chloroplast evolution show that incomplete lineage sorting cannot explain these patterns in most cases. Instead, most of the observed discordance is better explained by cytoplasmic introgression. Molecular tests of evolution further indicate that selection may have played a role in driving patterns of plastid variation - although additional experimental work is needed to fully evaluate the importance of selection on organellar variants in different parts of the geographic range. Overall, this study represents one of the most comprehensive tests of the drivers of cytonuclear discordance and highlights the potential for gene flow to lead to extensive organellar introgression in hybridizing taxa.

Skim-Sequencing Reveals the Likely Origin of the Enigmatic Endangered Sunflower Helianthus schweinitzii

“…In this study, the chloroplast phylogeny did not recover any perennial Helianthus species as reciprocally monophyletic. This is in line with previous findings in other perennial Helianthus [21] as well as in annual Helianthus taxa [52]. These results can be explained by incomplete lineage sorting (ILS) or by reticulation.…”

“…These associations reflect historical organelle capture events occurring among pairs of taxa that are interfertile [56]. Previous results in annual Helianthus [52] have indicated that, relative to ILS, reticulation is likely more important in generating patterns of cytonuclear discordance such as those observed here. Indeed, we identified several cases of haplotype sharing among geographically proximate populations (Figure 2), which would indicate that hybridization is more likely than ILS.…”

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…Potential cytoplasmic introgression driven by selection among Helianthus species was also reported, leading to widespread CN discordance in genealogies [77]. Selection might shape the pattern of organellar variation for some specific genes, resulting in adaptive introgression of the plastid genomes favoring local adaptation [77]. Cytoplasmic genomes can be important capacitors for the generation of novel phenotypes in specific environments, as shown in a study on Arabidopsis thaliana [42].…”

“…They revealed that the cytoplasms of these species were adapted to each specific habitat, suggesting that variation in the organellar genome could contribute to local adaptation and ecological differentiation [76]. Potential cytoplasmic introgression driven by selection among Helianthus species was also reported, leading to widespread CN discordance in genealogies [77]. Selection might shape the pattern of organellar variation for some specific genes, resulting in adaptive introgression of the plastid genomes favoring local adaptation [77].…”

Massive haplotypes underlie ecotypic differentiation in sunflowers

“…The call set included the 1518 samples described above, the Sunflower Association Mapping (SAM) population (a set of cultivated H. annuus lines 54 ), and wild Helianthus samples previously sequenced for other projects [54][55][56] , for a total of 2392 samples (Supplementary Table 1). The additional samples were included to improve SNP calling, and to identify haploblock genotypes.…”