Reconstructing the Complex Evolutionary History of the Papuasian Schefflera Radiation Through Herbariomics

Abstract

With its large proportion of endemic taxa, complex geological past, and location at the confluence of the highly diverse Malesian and Australian floristic regions, Papuasia-the floristic region comprising the Bismarck Archipelago, New Guinea, and the Solomon Islands-represents an ideal natural experiment in plant biogeography. However, scattered knowledge of its flora and limited representation in herbaria have hindered our understanding of the drivers of its diversity. Focusing on the woody angiosperm genus Schefflera (Araliaceae), we ask whether its morphologically defined infrageneric groupings are monophyletic, when these lineages diverged, and where (within Papuasia or elsewhere) they diversified. To address these questions, we use a high-throughput sequencing approach (Hyb-Seq) which combines target capture (with an angiosperm-wide bait kit targeting 353 single-copy nuclear loci) and genome shotgun sequencing (which allows retrieval of regions in high-copy number, e.g., organellar DNA) of historical herbarium collections. To reconstruct the evolutionary history of the genus we reconstruct molecular phylogenies with Bayesian inference, maximum likelihood, and pseudo-coalescent approaches, and co-estimate divergence times and ancestral areas in a Bayesian framework. We find strong support for most infrageneric morphological groupings, as currently circumscribed, and we show the efficacy of the Angiosperms-353 probe kit in resolving both deep and shallow phylogenetic relationships. We infer a sequence of colonization to explain the present-day distribution of Schefflera in Papuasia: from the Sunda Shelf, Schefflera arrived to the Woodlark plate (presentday eastern New Guinea) in the late Oligocene (when most of New Guinea was submerged) and, subsequently (throughout the Miocene), it migrated westwards (to the Maoke and Bird's Head Plates and thereon) and further diversified, in agreement with previous reconstructions.

Niche evolution of the Neotropical tree genusOtobain the context of global biogeography of the nutmeg family, Myristicaceae

“…Even though current short-read sequencing techniques perform well with herbarium specimens as compared to conventional Sanger sequencing (Bakker et al, 2015), the level of degradation common among wet tropical specimens led (Brewer et al, 2019) to recommend the use of silica tissue for wet tropical groups. While we agree that this is a bestpractice, as in other herbarium-based studies (Brewer et al, 2019;Shee et al, 2020), we were able to extract useful phylogenomic data from herbarium specimens using Angiosperms353.…”

“…Hybrid-enriched target sequence capture with Angiosperms353 has proven useful for generating phylogenetically informative data at multiple taxonomic scales and from different sources of DNA (i.e., silica-dried tissue versus herbarium specimens; (Brewer et al, 2019;Shee et al, 2020;Valderrama et al, 2020). To our knowledge, our study represents a new milestone for Angiosperms353 phylogenomics: the first exclusively herbariomic dataset for a wet tropical genus.…”

Strategies for reducing per‐sample costs in target capture sequencing for phylogenomics and population genomics in plants

“…Extra modifications (recommended when polysaccharides and secondary metabolites are abundant) include sorbitol and high‐salt (4 M NaCl) CTAB (e.g., for mucilage‐rich tissue, Tel‐Zur et al., ; Štorchová et al., ) or 2% polyvinylpyrrolidone (PVP) (e.g., for latex‐rich tissue, Michiels et al., ). When phenol use is restricted (e.g., in light of health and safety concerns), additional clean‐up steps are recommended, such as column (e.g., CsCl‐EtBr density gradient centrifugation, Albach and Chase, ; Ahmed et al., ; Höpke et al., ) or bead cleaning (e.g., solid‐phase reversible immobilization [e.g., SPRIselect beads, Beckman Coulter, Indianapolis, Indiana, USA]; Shee et al., ), and even additional modified CTAB protocols optimized for plant lineages with high levels of polysaccharides and secondary metabolites (Štorchová et al., ; Sahu et al., ).…”

On the potential of Angiosperms353 for population genomics

“…The feasibility of estimating demographic parameters (including heterozygosity, effective population size, and levels of introgression) in non-model taxa relies on markers that can detect sufficient variation across the genome while remaining cost-effective for analysis on hundreds of individuals. In plants, population genomics could benefit from markers that enable the further unlocking of herbarium specimens for botanical research, following advances in phylogenomics (Shee et al, 2020), microbiome research (Heberling and Burke, 2019), and the effects of climate change on plant populations (Miller-Rushing et al, 2009).…”