Owens Gregory L, Cai Zhe, Bercovich Natalia, Todesco Marco, Lee-Yaw Julie A, Rieseberg Loren H
Department of Biology, University of Victoria, Victoria, BC V8W 2Y2, Canada.
Department of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
Proc Natl Acad Sci U S A. 2025 Aug 5;122(31):e2410943122. doi: 10.1073/pnas.2410943122. Epub 2025 Jul 28.
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 , 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.
植物和动物的细胞质基因组常常无法遵循物种界限。然而，导致这种模式的机制却鲜为人知，部分原因是很少有研究将细胞质变异与表型性状或环境差异联系起来。在此，我们使用了1554个先前发表的以及185个新的全基因组序列，这些序列代表了向日葵属的14个分类单元，在共同园圃中测量了91个表型性状，并收集了39个环境变量，以测试细胞质基因组变异的环境和表型效应。与之前的研究一致，在多个物种中发现了两个不同的叶绿体分支，物种间叶绿体分支的共享主要是由于反复的基因渗入而非不完全谱系分选。还发现了两个线粒体分支，其中98%的个体的线粒体分支与叶绿体分支相匹配，这意味着两个基因组主要都是母系遗传。细胞质分支与多个物种的种子形状差异有关，可能也与干旱有关，这表明其在局部适应中发挥了作用。相反，基于叶绿体和核变异之间的关联，我们没有发现任何可靠的核质相互作用。综合来看，这项研究表明一年生向日葵的细胞质基因组代表了一种跨物种平衡多态性，这种多态性可能是通过适应不同环境而得以维持。更广泛地说，我们的结果证实了整合种概念，展示了即使跨越非常强大的生殖屏障的基因渗入如何促进一个物种复合体的环境适应。
