skip to main content

Title: Phylogenomics of the genus Populus reveals extensive interspecific gene flow and balancing selection

Phylogenetic analysis is complicated by interspecific gene flow and the presence of shared ancestral polymorphisms, particularly those maintained by balancing selection. In this study, we aimed to examine the prevalence of these factors during the diversification ofPopulus, a model tree genus in the Northern Hemisphere.

We constructed phylogenetic trees of 29Populustaxa using 80 individuals based on re‐sequenced genomes. Our species tree analyses recovered four main clades in the genus based on consensus nuclear phylogenies, but in conflict with the plastome phylogeny. A few interspecific relationships remained unresolved within the multiple‐species clade because of inconsistent gene trees. Our results indicated that gene flow has been widespread within each clade and also occurred among the four clades during their early divergence.

We identified 45 candidate genes with ancient polymorphisms maintained by balancing selection. These genes were mainly associated with mating compatibility, growth and stress resistance.

Both gene flow and selection‐mediated ancient polymorphisms are prevalent in the genusPopulus. These are potentially important contributors to adaptive variation. Our results provide a framework for the diversification of model tree genus that will facilitate future comparative studies.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
New Phytologist
Page Range / eLocation ID:
p. 1370-1382
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The genusLiriomyzaMik (Diptera: Agromyzidae) is a diverse and globally distributed group of acalyptrate flies. Phylogenetic relationships amongLiriomyzaspecies have remained incompletely investigated and have never been fully addressed using molecular data. Here, we reconstruct the phylogeny of the genusLiriomyzausing various phylogenetic methods (maximum likelihood, Bayesian inference, and gene tree coalescence) on target‐capture‐based phylogenomic datasets (nucleotides and amino acids) obtained from anchored hybrid enrichment (AHE). We have recovered tree topologies that are nearly congruent across all data types and methods, and individual clade support is strong across all phylogenetic analyses. Moreover, defined morphological species groups and clades are well‐supported in our best estimates of the molecular phylogeny.Liriomyza violivora(Spencer) is a sister group to all remaining sampledLiriomyzaspecies, and the well‐known polyphagous vegetable pests [L. huidobrensis(Blanchard),L. langeiFrick,L. bryoniae.(Kaltenbach),L. trifolii(Burgess),L. sativaeBlanchard, andL. brassicae(Riley)]. belong to multiple clades that are not particularly closely related on the trees. Often, closely relatedLiriomyzaspecies feed on distantly related host plants. We reject the hypothesis that cophylogenetic processes betweenLiriomyzaspecies and their host plants drive diversification in this genus. Instead,Liriomyzaexhibits a widespread pattern of major host shifts across plant taxa. Our new phylogenetic estimate forLiriomyzaspecies provides considerable new information on the evolution of host‐use patterns in this genus. In addition, it provides a framework for further study of the morphology, ecology, and diversification of these important flies.

    more » « less
  2. Summary

    The tree of life is highly reticulate, with the history of population divergence emerging from populations of gene phylogenies that reflect histories of introgression, lineage sorting and divergence. In this study, we investigate global patterns of oak diversity and test the hypothesis that there are regions of the oak genome that are broadly informative about phylogeny.

    We utilize fossil data and restriction‐site associatedDNAsequencing (RAD‐seq) for 632 individuals representing nearly 250Quercusspecies to infer a time‐calibrated phylogeny of the world's oaks. We use a reversible‐jump Markov chain Monte Carlo method to reconstruct shifts in lineage diversification rates, accounting for among‐clade sampling biases. We then map the > 20 000RAD‐seq loci back to an annotated oak genome and investigate genomic distribution of introgression and phylogenetic support across the phylogeny.

    Oak lineages have diversified among geographic regions, followed by ecological divergence within regions, in the Americas and Eurasia. Roughly 60% of oak diversity traces back to four clades that experienced increases in net diversification, probably in response to climatic transitions or ecological opportunity.

    The strong support for the phylogeny contrasts with high genomic heterogeneity in phylogenetic signal and introgression. Oaks are phylogenomic mosaics, and their diversity may in fact depend on the gene flow that shapes the oak genome.

    more » « less
  3. Abstract

    Despite the economic, ecological, and scientific importance of the genera Salix L. (willows) and Populus L. (poplars, cottonwoods, and aspens) Salicaceae, we know little about the sources of differences in species diversity between the genera and of the phylogenetic conflict that often confounds estimating phylogenetic trees. Salix subgenera and sections, in particular, have been difficult to classify, with one recent attempt termed a “spectacular failure” due to a speculated radiation of the subgenera Vetrix and Chamaetia. Here, we use targeted sequence capture to understand the evolutionary history of this portion of the Salicaceae plant family. Our phylogenetic hypothesis was based on 787 gene regions and identified extensive phylogenetic conflict among genes. Our analysis supported some previously described subgeneric relationships and confirmed the polyphyly of others. Using an fbranch analysis, we identified several cases of hybridization in deep branches of the phylogeny, which likely contributed to discordance among gene trees. In addition, we identified a rapid increase in diversification rate near the origination of the Vetrix–Chamaetia clade in Salix. This region of the tree coincided with several nodes that lacked strong statistical support, indicating a possible increase in incomplete lineage sorting due to rapid diversification. The extraordinary level of both recent and ancient hybridization in both Salix and Populus have played important roles in the diversification and diversity in these two genera.

    more » « less
  4. Premise

    Cornales is an order of flowering plants containing ecologically and horticulturally important families, including Cornaceae (dogwoods) and Hydrangeaceae (hydrangeas), among others. While many relationships in Cornales are strongly supported by previous studies, some uncertainty remains with regards to the placement of Hydrostachyaceae and to relationships among families in Cornales and within Cornaceae. Here we analyzed hundreds of nuclear loci to test published phylogenetic hypotheses and estimated a robust species tree for Cornales.


    Using the Angiosperms353 probe set and existing data sets, we generated phylogenomic data for 158 samples, representing all families in the Cornales, with intensive sampling in the Cornaceae.


    We curated an average of 312 genes per sample, constructed maximum likelihood gene trees, and inferred a species tree using the summary approach implemented in ASTRAL‐III, a method statistically consistent with the multispecies coalescent model.


    The species tree we constructed generally shows high support values and a high degree of concordance among individual nuclear gene trees. Relationships among families are largely congruent with previous molecular studies, except for the placement of the nyssoids and the Grubbiaceae‐Curtisiaceae clades. Furthermore, we were able to place Hydrostachyaceae within Cornales, and within Cornaceae, the monophyly of known morphogroups was well supported. However, patterns of gene tree discordance suggest potential ancient reticulation, gene flow, and/or ILS in the Hydrostachyaceae lineage and the early diversification ofCornus. Our findings reveal new insights into the diversification process across Cornales and demonstrate the utility of the Angiosperms353 probe set.

    more » « less
  5. Abstract Aim

    To test the importance of alternative diversification drivers and biogeographical processes for the evolution of Amazonian upland forest birds through a densely sampled analysis of diversification of the endemic Amazonian genusRhegmatorhinaat multiple taxonomic and temporal scales.




    Antbirds (Thamnophilidae).


    We sequenced four mtDNAand nuclear gene regions of 120 individuals from 50 localities representing all recognized species and subspecies of the genus. We performed molecular phylogenetic analyses using both gene tree and species tree methods, molecular dating analysis and estimated population demographic history and gene flow.


    Dense sampling throughout the distribution ofRhegmatorhinarevealed that the main Amazonian rivers delimit the geographic distribution of taxa as inferred from mtDNAlineages. Molecular phylogenetic analyses resulted in a strongly supported phylogenetic hypothesis for the genus, with two main clades currently separated by the Madeira River. Molecular dating analysis indicated diversification during the Quaternary. Reconstruction of recent demographic history of populations revealed a trend for population expansion in eastern Amazonia and stability in the west. Estimates of gene flow corroborate the possibility that migration after divergence had some influence on the current patterns of diversity.

    Main Conclusions

    Based on broad‐scale sampling, a clarification of taxonomic boundaries, and strongly supported phylogenetic relationships, we confirm that, first, mitochondrial lineages within this upland forest Amazonian bird genus agree with spatial patterns known for decades based on phenotypes, and second, that most lineages are geographically delimited by the large Amazonian rivers. The association between past demographic changes related to palaeoclimatic cycles and the historically varying strength and size of rivers as barriers to dispersal may be the path to the answer to the long‐standing question of identifying the main drivers of Amazonian diversification.

    more » « less