Complex History of Organellar Introgression in Nothofagus Trees: Chloroplast and Mitochondrial Capture Facilitated by...

Hybridization is widespread across diverse groups of organisms, and in some cases, organellar genomes of one species become fixed in another following hybridization and backcrossing, a phenomenon known as organelle capture. Because cytoplasmic genomes can contribute to local adaptation, organelle capture has the potential to confer a selective advantage and may be maintained by natural selection. Here, we evaluate this hypothesis in Nothofagus trees by analyzing chloroplast and mitochondrial genomes. Organellar phylogenies consistently separate individuals by geography rather than by species, with the two main clades mostly divided into northern and southern groups with a boundary at about 42° S, a pattern not captured by traditional nuclear markers. This major split is estimated to have originated during Pleistocene glaciations, when contraction into refugia and postglacial expansion may have been facilitated by hybridization. Chloroplast genes show signatures of positive selection in protein-coding genes, with most signals concentrated in the northern clade. These results are consistent with potential adaptation to latitudinal and environmental gradients. In contrast, mitochondrial genes remain conserved under purifying selection, suggesting that mitochondrial patterns may be consistent with co-introgression alongside chloroplasts. This pattern is consistent with the predominant maternal inheritance of both organelles in angiosperms, unlike gymnosperms where mitochondria are usually maternally and chloroplasts paternally inherited, a difference that may shape organelle capture dynamics. Overall, our results are consistent with a potential pattern of organelle co-introgression involving the simultaneous introgression of chloroplast and mitochondrial genomes through hybridization. These findings provide a framework for exploring the evolutionary significance of organelle introgression and its potential role in local adaptation and speciation in trees.