Different rates of pollen and seed gene flow cause branch-length and geographic cytonuclear discordance within Asian butternuts

Topological cytonuclear discordance is commonly observed in plant phylogenetic and phylogeographic studies, yet few studies have attempted to detect two other forms of cytonuclear discordance (branch length and geographical) and to uncover the causes of the discordance. We used the whole nuclear and chloroplast genome data from 80 individual Asian butternuts to reveal the pattern and processes of cytonuclear discordance. Our findings indicate that the chloroplast genome had substantially deeper divergence (branch-length discordance) and a steeper cline in the contact zone (geographic discordance) compared with the nuclear genome. After various hypothesis have been tested, the results suggest that incomplete lineage sorting, positive selection and cytonuclear incompatibility are probably insufficient to explain this pattern. However, isolation-by-distance analysis and gene flow estimation point to a much higher level of gene flow by pollen compared with by seeds, which may have slowed down lineage divergence and mediated wider contact for nuclear genome compared with the chloroplast genome. Altogether, this study highlights a critical role of sex-biased dispersal in causing discordance between the nuclear and plastid genome of Asian butternuts. Given its ubiquity among plants, asymmetric gene flow should be given a high priority in future studies of cytonuclear discordance.

Automated summary

This study reveals that in Asian butternuts, the chloroplast genome shows deeper discordance compared to the nuclear genome, as well as steeper geographic discordance in the contact zone. This suggests a critical role of sex-biased dispersal in causing discordance between the nuclear and plastid genome of Asian butternuts, highlighting the importance of considering asymmetric gene flow in future studies of cytonuclear discordance.