Embracing heterogeneity: coalescing the Tree of Life and the future of phylogenomics

PeerJ. 2019 Feb 14;7:e6399. doi: 10.7717/peerj.6399. eCollection 2019.

Abstract

Building the Tree of Life (ToL) is a major challenge of modern biology, requiring advances in cyberinfrastructure, data collection, theory, and more. Here, we argue that phylogenomics stands to benefit by embracing the many heterogeneous genomic signals emerging from the first decade of large-scale phylogenetic analysis spawned by high-throughput sequencing (HTS). Such signals include those most commonly encountered in phylogenomic datasets, such as incomplete lineage sorting, but also those reticulate processes emerging with greater frequency, such as recombination and introgression. Here we focus specifically on how phylogenetic methods can accommodate the heterogeneity incurred by such population genetic processes; we do not discuss phylogenetic methods that ignore such processes, such as concatenation or supermatrix approaches or supertrees. We suggest that methods of data acquisition and the types of markers used in phylogenomics will remain restricted until a posteriori methods of marker choice are made possible with routine whole-genome sequencing of taxa of interest. We discuss limitations and potential extensions of a model supporting innovation in phylogenomics today, the multispecies coalescent model (MSC). Macroevolutionary models that use phylogenies, such as character mapping, often ignore the heterogeneity on which building phylogenies increasingly rely and suggest that assimilating such heterogeneity is an important goal moving forward. Finally, we argue that an integrative cyberinfrastructure linking all steps of the process of building the ToL, from specimen acquisition in the field to publication and tracking of phylogenomic data, as well as a culture that values contributors at each step, are essential for progress.

Keywords: Gene flow; Genome; Multispecies coalescent model; Retroelement; Speciation; Transcriptome.

Grant support

The Gothenburg Center for Advanced Studies (GoCas) workshop ‘Origins of Biodiversity’ was funded by Chalmers University of Technology and the University of Gothenburg. The authors are supported by scholarships or research grants from the following agencies: Swedish Research Council (Bengt Oxelman, Alexandre Antonelli); U.S. National Science Foundation; European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013, ERC Grant Agreement n. 331024 to Alexandre Antonelli); Swedish Foundation for Strategic Research; Wallenberg Academy Fellowship (Alexandre Antonelli); Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (Fernanda P. Werneck); Partnerships for Enhanced Engagement in Research from the U.S. National Academy of Sciences (Fernanda P. Werneck); U.S. Agency of International Development—PEER NAS/USAID (Fernanda P. Werneck); and L’Oreal-Unesco For Women in Science Program (Fernanda P. Werneck). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.