Abstract
The carnivorous members of the large, hyperdiverse Caryophyllales (e.g., Venus flytrap, sundews, and Nepenthes pitcher plants) represent perhaps the oldest and most diverse lineage of carnivorous plants. However, despite numerous studies seeking to elucidate their evolutionary relationships, the early-diverging relationships remain unresolved. To explore the utility of phylogenomic data sets for resolving relationships among the carnivorous Caryophyllales, we sequenced 10 transcriptomes, including all the carnivorous genera except those in the rare West African liana family Dioncophyllaceae. We used a variety of methods to infer the species tree, examine gene tree conflict, and infer paleopolyploidy events. Phylogenomic analyses supported the monophyly of the carnivorous Caryophyllales, with a crown age of 68-83 million years. In contrast to previous analyses, we recovered the remaining noncore Caryophyllales as nonmonophyletic, although the node supporting this relationship contained a significant amount of gene tree discordance. We present evidence that the clade contains at least seven independent paleopolyploidy events, previously unresolved nodes from the literature have high levels of gene tree conflict, and taxon sampling influences topology even in a phylogenomic data set, regardless of the use of coalescent or supermatrix methods. Our data demonstrate the importance of carefully considering gene tree conflict and taxon sampling in phylogenomic analyses. Moreover, they provide a remarkable example of the propensity for paleopolyploidy in angiosperms, with at least seven such events in a clade of less than 2500 species.
Highlights
Carnivory in plants has long fascinated both the general public and evolutionary biologists
We present the first phylogenomic analysis focused on the noncore Caryophyllales, with sampling that covers all genera of carnivorous Caryophyllales except the poorly studied and rare lianas in the family Dioncophyllaceae of West Africa
In the case of the data set containing all taxa (AA all taxa included (ALLTAX)), the branch supporting Frankeniaceae+Tamaricaceae as the lineage sister to everything else showed a large amount of conflict with ~15.4% of genes supporting the topology, ~14.6% supporting a dominate alternate topology of a monophyletic noncarnivorous noncore (NCNC), ~25% supporting other alternate topologies, and
Summary
Carnivory in plants has long fascinated both the general public and evolutionary biologists. Despite broad appeal and interest, the evolutionary relationships in the noncore Caryophyllales remain ambiguous, with studies seeking to resolve these relationships often resulting in individually wellsupported but mutually conflicting topologies (Meimberg et al, 2000; Cameron et al, 2002; Brockington et al, 2009; HernándezLedesma et al, 2015). The strong support for conflicting topologies from different studies may be explained by the reliance on one or a few genes leading to systematic error (Maddison, 1997; Rokas et al, 2003) This type of error can arise from a variety of sources, including, but not limited to, incomplete lineage sorting, horizontal gene transfer, hybridization, and hidden paralogy (Galtier and Daubin, 2008). Analyses of gene tree concordance and conflict allow for a better understanding of the formation of species relationships and the complexity that arises in genomes as a result of speciation (Pease et al, 2016)
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