Resolving Recalcitrant Clades in the Pantropical Ochnaceae: Insights From Comparative Phylogenomics of Plastome and Nuclear Genomic Data Derived From Targeted Sequencing

Abstract

Plastid DNA sequence data have been traditionally widely used in plant phylogenetics because of the high copy number of plastids, their uniparental inheritance, and the blend of coding and non-coding regions with divergent substitution rates that allow the reconstruction of phylogenetic relationships at different taxonomic ranks. In the present study, we evaluate the utility of the plastome for the reconstruction of phylogenetic relationships in the pantropical plant family Ochnaceae (Malpighiales). We used the off-target sequence read fraction of a targeted sequencing study (targeting nuclear loci only) to recover more than 100 kb of the plastid genome from the majority of the more than 200 species of Ochnaceae and all but two genera using de novo and reference-based assembly strategies. Most of the recalcitrant nodes in the family’s backbone were resolved by our plastome-based phylogenetic inference, corroborating the most recent classification system of Ochnaceae and findings from a phylogenomic study based on nuclear loci. Nonetheless, the phylogenetic relationships within the major clades of tribe Ochnineae, which comprise about two thirds of the family’s species diversity, received mostly low support. Generally, the phylogenetic resolution was lowest at the infrageneric level. Overall there was little phylogenetic conflict compared to a recent analysis of nuclear loci. Effects of taxon sampling were invoked as the most likely reason for some of the few well-supported discords. Our study demonstrates the utility of the off-target fraction of a target enrichment study for assembling near-complete plastid genomes for a large proportion of samples.

Predominantly Eastward Long-Distance Dispersal in Pantropical Ochnaceae Inferred From Ancestral Range Estimation and Phylogenomics

“…and Sauvagesia s.l. which were shown to be poly-/paraphyletic in recent studies (Schneider et al, 2020(Schneider et al, , 2021, both still with the necessary nomenclatural changes pending. In Campylospermum, only Clade B sensu Schneider et al (2020) has a disjunct distribution in the present study.…”

“…We used our previously published datasets obtained from target enrichment of nuclear loci and indirectly captured nearcomplete plastid genomes based on an Ochnaceae-specific bait kit (Schneider et al, 2020(Schneider et al, , 2021Shah et al, 2021) but used a reduced taxon set to include only representative taxa that were needed for addressing our biogeographical questions. Reducing the number of taxa also facilitated the divergence time estimation, with far less computational time required for reaching convergence during the analyses (see below).…”

“…Both comprised 59 species each including one outgroup but with slightly different species composition. Some species were represented by different individuals because of excessive missing data in one of the datasets (as outlined in Schneider et al, 2020Schneider et al, , 2021; Supplementary Table 1). The nuclear alignment comprised 77,940 bp and the plastid alignment 117,923 bp.…”

“…500 spp. ; Amaral and Bittrich, 2014;Schneider et al, 2020Schneider et al, , 2021. The latter is subdivided into four tribes (Schneider et al, 2014), with the monotypic Testuleeae confined to tropical Africa, Luxemburgieae being endemic to the Neotropics, and Sauvagesieae and Ochneae being pantropical.…”

“…Moreover, the infrageneric sampling was insufficient to infer the ancestral range for several genera with disjunct distributions, including those for which delimitation and monophyly were unclear. Recently, phylogenomic studies based on nuclear loci and plastome data (Schneider et al, 2020(Schneider et al, , 2021 and by far with the most complete taxon sampling to date provided the required framework for tackling questions about the spatiotemporal diversification of Ochnaceae. Thus, the aim of this study is to obtain estimates of divergence time for Ochnaceae to uncover the ancestral range, the mechanisms that have guided its extant pantropical distribution, and the direction of its dispersal at deep and shallow times.…”