A trans-species cytoplasmic polymorphism is associated with seed shape and aridity across multiple species of...

The cytoplasmic genomes of plants and animals often fail to track species boundaries. However, the mechanisms responsible for such patterns are poorly understood, in part because few studies have linked cytoplasmic variation to phenotypic traits or environmental differences. Here, we use 1,554 previously published and 185 new whole genome sequences representing 14 taxa from the sunflower genus Helianthus, 91 phenotypic traits measured in common gardens, and 39 environmental variables to test for environmental and phenotypic effects of cytoplasmic genome variation. In agreement with previous work, two distinct chloroplast clades were found across multiple species and the sharing of chloroplast clades between species was mainly due to repeated introgression rather than incomplete lineage sorting. Two mitochondrial clades were also found that matched the chloroplast clades for 98% of individuals, implying predominantly maternal inheritance of both genomes. Cytoplasmic clade was associated with differences in seed shape across several species, and likely with aridity, suggestive of a role in local adaptation. Conversely, we failed to find any credible cytonuclear interactions based on associations between chloroplast and nuclear variation. Taken together, this work suggests that cytoplasmic genomes in annual sunflowers represent a trans-species balanced polymorphism that is likely maintained by adaptation to different environments. More broadly, our results corroborate the syngameon concept, showing how introgression across even very strong reproductive barriers can facilitate environmental adaptation across a species complex.