Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales

Abstract

The angiosperm order Malpighiales includes ∼16,000 species and constitutes up to 40% of the understory tree diversity in tropical rain forests. Despite remarkable progress in angiosperm systematics during the last 20 y, relationships within Malpighiales remain poorly resolved, possibly owing to its rapid rise during the mid-Cretaceous. Using phylogenomic approaches, including analyses of 82 plastid genes from 58 species, we identified 12 additional clades in Malpighiales and substantially increased resolution along the backbone. This greatly improved phylogeny revealed a dynamic history of shifts in net diversification rates across Malpighiales, with bursts of diversification noted in the Barbados cherries (Malpighiaceae), cocas (Erythroxylaceae), and passion flowers (Passifloraceae). We found that commonly used a priori approaches for partitioning concatenated data in maximum likelihood analyses, by gene or by codon position, performed poorly relative to the use of partitions identified a posteriori using a Bayesian mixture model. We also found better branch support in trees inferred from a taxon-rich, data-sparse matrix, which deeply sampled only the phylogenetically critical placeholders, than in trees inferred from a taxon-sparse matrix with little missing data. Although this matrix has more missing data, our a posteriori partitioning strategy reduced the possibility of producing multiple distinct but equally optimal topologies and increased phylogenetic decisiveness, compared with the strategy of partitioning by gene. These approaches are likely to help improve phylogenetic resolution in other poorly resolved major clades of angiosperms and to be more broadly useful in studies across the Tree of Life. M alpighiales are one of the most surprising clades discovered in broad molecular phylogenetic studies of the flowering plants (1-3). The order contains ∼16,000 species and 42 families (2, 3) that exhibit remarkable morphological and ecological diversity. A few examples include cactus-like succulents (Euphorbiaceae), epiphytes (Clusiaceae), holoparasites (Rafflesiaceae), submerged aquatics (Podostemaceae), and windpollinated trees (temperate Salicaceae). The order is ecologically important: species in Malpighiales constitute up to 40% of the understory tree diversity in tropical rain forests worldwide (4). They also include many economically important species, such as Barbados nut (Jatropha curcas L., Euphorbiaceae), cassava (Manihot esculenta Crantz, Euphorbiaceae), castor bean (Ricinus communis L., Euphorbiaceae), coca (Erythroxylum coca Lam., Erythroxylaceae), flax (Linum usitatissimum L., Linaceae), the poplars (Populus spp., Salicaceae), and the rubber tree (Hevea brasiliensis Müll. Arg., Euphorbiaceae). Partially for this reason, genomic resources for Malpighiales are growing at a rapid pace and include whole-genome sequencing projects completed or near completion for Barbados nut (5), cassava, castor bean (6), flax, and poplar (7). Thus, a resolved phylogeny of Malpighiales is critical not only for evol...

Long-term morphological stasis maintained by a plant–pollinator mutualism

“…Results from our analyses (Fig. S1) were identical to recent studies but were better supported in key parts of the phylogeny (21,28). Here, Elatinaceae + Malpighiaceae is established as a well-supported (86 maximum-likelihood bootstrap percentage, 1.0 Bayesian posterior probability) sister clade to Centroplacaceae.…”

“…Here, we analyze morphological diversification patterns in Malpighiaceae to test the hypothesis that floral morphological stasis is driven and maintained by their specialist oil-bee pollinators. This finding may in turn shed light on the significant increase in net species diversification rate that coincided with the origin of the Malpighiaceae and their pollinator mutualism (21).…”

The rubber tree genome reveals new insights into rubber production and species adaptation

“…The divergence time for the Euphorbiaceae family is estimated to be 57.7 Myr ago (Fig. 1d) G e n e fa m il y O r p h a n s G e n e s in fa m il y T o ta l g e n e s reported dating of 89.9 Myr ago 14 , possibly because of the limited number of Euphorbiaceae species used here.…”

“…The most ancient peak, representing γ duplication, is rather obscure and mingled with the right peak. A recent phylogenomic analyses inferred the clades Euphorbiaceae (Hevea, Manihot), Salicaceae (Populus) and Linaceae (Linum) to have emerged 89.9, 58.0 and 39.5 Myr ago, respectively 14 . Hence, Linum is the youngest of the five species, as also reflected by its lower K s and 4DTv peak values (Fig.…”

Erythroxylum (Erythroxylaceae) na Mata Atlântica da Bahia, Brasil

“…A família já foi incluída na ordem Linales por Cronquist (1981), porém recentes estudos moleculares e morfológicos apontaram o táxon como grupo irmão de Rhizophoraceae (Wurdack & Davis 2009;Xi et al 2012), assegurando sua posição dentro da ordem Malpighiales.…”