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

Lin‐Lin Xu,Rui‐Min Yu,Bo‐Wen Zhang,Xin‐Rui Lin,Wei‐Ning Bai,Kui Lin,Nan Li,Da‐Yong Zhang

doi:10.1111/nph.17564

Lin‐Lin Xu, Rui‐Min Yu + Show 6 more

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https://doi.org/10.1111/nph.17564

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Abstract

Summary 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.

Highlights

Cytonuclear discordance refers to markedly different phylogenetic patterns between nuclear and organelle markers, and is a common phenomenon in genealogical discordance (Rieseberg & Soltis, 1991; Toews & Brelsford, 2012)
The analyses described so far provided strong evidence for gene flow between species of Asian butternuts; evaluating divergence time using strictly bifurcating tree methods was improper because gene flow can result in underestimates of species divergence time (Leache et al, 2014)
A point estimate of the divergence time between the two clades was dated to 6.80 million years ago (Ma) (95% highest posterior density (HPD): 4.24–9.58 Ma); the divergence time for all 16 haplotypes of J. cathayensis was 1.99 Ma (95% HPD: 1.15–2.9 Ma), and that for five haplotypes of J. mandshurica and J. ailantifolia was 3.50 Ma (95% HPD: 2.03–5.27 Ma, Fig. 1a)

Summary

Introduction

Cytonuclear discordance refers to markedly different phylogenetic patterns between nuclear and organelle (chloroplast or mitochondria) markers, and is a common phenomenon in genealogical discordance (Rieseberg & Soltis, 1991; Toews & Brelsford, 2012). Branch-length discordance involves cases in which the organelle genome is inferred to have substantially deeper divergence, whereas the nuclear genome shows relatively little or no divergence This discordance is often reported in animals, such as birds (Hogner et al, 2012; Pavlova et al, 2013), amphibia (Firneno et al, 2020) and reptiles (Singhal & Moritz, 2012), but rarely in plants (but see Huang et al, 2014). It is worth noting that even in cases when topological discordance does not occur, branch-length and geographic discordance can still be observed and have non-negligible influence on evolutionary history analyses They indicate historical and demographic complexities in phylogeographic analysis and can prevent establishing conclusive taxonomies (Bonnet et al, 2017) and bias the estimation of species divergence time with chloroplast DNA (Huang et al, 2014)

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