Phylogenomic incongruence, hypothesis testing, and taxonomic sampling: The monophyly of characiform fishes*

Abstract

Phylogenomic studies using genome‐wide datasets are quickly becoming the state of the art for systematics and comparative studies, but in many cases, they result in strongly supported incongruent results. The extent to which this conflict is real depends on different sources of error potentially affecting big datasets (assembly, stochastic, and systematic error). Here, we apply a recently developed methodology (GGI or gene genealogy interrogation) and data curation to new and published datasets with more than 1000 exons, 500 ultraconserved element (UCE) loci, and transcriptomic sequences that support incongruent hypotheses. The contentious non‐monophyly of the order Characiformes proposed by two studies is shown to be a spurious outcome induced by sample contamination in the transcriptomic dataset and an ambiguous result due to poor taxonomic sampling in the UCE dataset. By exploring the effects of number of taxa and loci used for analysis, we show that the power of GGI to discriminate among competing hypotheses is diminished by limited taxonomic sampling, but not equally sensitive to gene sampling. Taken together, our results reinforce the notion that merely increasing the number of genetic loci for a few representative taxa is not a robust strategy to advance phylogenetic knowledge of recalcitrant groups. We leverage the expanded exon capture dataset generated here for Characiformes (206 species in 23 out of 24 families) to produce a comprehensive phylogeny and a revised classification of the order.

Ancient and contingent body shape diversification in a hyperdiverse continental fish radiation

“…S1 for details) and repeated all macroevolutionary analyses using that constrained phylogeny. We did not repeat analysis with a phylogeny constrained to the very recent reconstruction of Betancur-R et al (2018), because that paper appeared while our contribution was in the final stages of revision after peer review.…”

Digest: Resolving phylogenomic conflicts in characiform fishes†

“…At least in this case, the use of denser taxon coverage appears to be more important than sequencing a large number of genes to resolve phylogenomic conflicts. Betancur-R et al (2019) also show that currently accepted methods for analyzing large datasets are outpaced by the sheer growth of data. Hence, presently applied techniques, when scaled up, struggle to handle phylogenomic analyses due to amplified biases and altered signal-noise ratios.…”

“…In this issue, by using Gene Genealogy Interrogation (GGI) in combination with a comprehensive exonic dataset, Betancur‐R et al. () resolved with high confidence the long‐debated monophyly of the fish order Characiformes (including suborders Characoidei and Citharinoidei; Topology “A”). The GGI approach applied to randomly‐assembled subsets of gene trees produced the correct monophyletic topology, while the same approach on subsampled datasets with fewer taxa frequently resolved resulted incongruent, non‐monophyletic topologies (H 03 and H 05 ).…”

“…Betancur‐R et al. () also show that currently accepted methods for analyzing large datasets are outpaced by the sheer growth of data. Hence, presently applied techniques, when scaled up, struggle to handle phylogenomic analyses due to amplified biases and altered signal–noise ratios.…”

“…In this issue, Betancur-R et al (2019) applied a recently developed hypothesis-testing approach, Gene Genealogy Interrogation (GGI), to reconcile conflicting phylogenomic inferences and to estimate the effect of taxon sampling. The authors focused on fishes of the order Characiformes, a clade with a longstanding taxonomic controversy (see Chen et al 2013) that has been resolved as either monophyletic or non-monophyletic by recent phylogenomic studies ( Fig.…”