Resolving Deep Nodes in an Ancient Radiation of Neotropical Fishes in the Presence of Conflicting Signals from Incomplete Lineage Sorting

Abstract

Resolving patterns of ancient and rapid diversifications is one of the most challenging tasks in evolutionary biology. These difficulties arise from confusing phylogenetic signals that are associated with the interplay of incomplete lineage sorting and homoplasy. Phylogenomic analyses of hundreds, or even thousands, of loci offer the potential to resolve such contentious relationships. Yet, how much useful phylogenetic information these large data sets contain remains uncertain and often goes untested. Here, we assess the utility of different data filtering approaches to maximize phylogenetic information and minimize noise when reconstructing an ancient radiation of Neotropical electric knifefishes (Order Gymnotiformes) using ultraconserved elements. We found two contrasting hypotheses of gymnotiform evolutionary relationships depending on whether phylogenetic inferences were based on concatenation or coalescent methods. In the first case, all analyses inferred a previously-and commonly-proposed hypothesis, where the family Apteronotidae was found as the sister group to all other gymnotiform families. In contrast, coalescent-based analyses suggested a novel hypothesis where families producing pulse-type (viz., Gymnotidae, Hypopomidae and Rhamphichthyidae) and wave-type electric signals (viz., Apteronotidae, Sternopygidae) were reciprocally monophyletic.Nodal support for this second hypothesis increased when analyzing loci with the highest phylogenetic information content and further increased when data were pruned using targeted filtering methods that maximized phylogenetic informativeness at the deepest nodes of the Gymnotiformes. Bayesian concordance analyses and topology tests of individual gene genealogies demonstrated that the difficulty of resolving this radiation was likely due to high gene-tree incongruences that resulted from incomplete lineage sorting. We show that data filtering reduces gene tree heterogeneity and increases nodal support and consistency of species Downloaded from https://academic.oup.com/sysbio/advance-article-abstract/doi/10.1093/sysbio/syy085/5232148 by Bukkyo University user on 06 December 20183 trees using coalescent methods; however, we failed to observe the same effect when using concatenation methods. Furthermore, the targeted filtering strategies applied here support the use of "gene data interrogation" rather than "gene genealogy interrogation" approaches in phylogenomic analyses, to extract phylogenetic signal from intractable portions of the Tree of Life.

Deciphering the Evolutionary History of Arowana Fishes (Teleostei, Osteoglossiformes, Osteoglossidae): Insight from Comparative Cytogenomics

“…Modern cytogenetic and genomic tools are central to inferring the evolutionary history of ancient fish lineages (e.g., References [3,34,35,36,37,38]). Such data, however, are still scarce for Osteoglossiformes, with Osteoglossidae being a typical example, thereby limiting our understanding of their genome and karyotype evolution ([39]; reviewed in References [35,40,41,42,43]).…”

A Target Enrichment Bait Set for Studying Relationships among Ostariophysan Fishes

“…These conflicts may arise from a very rapid diversification event that occurred around the origin of the Gymnotiformes which created an evolutionary history muddled by incomplete lineage sorting. The causes of these incongruences and methods to increase consistency in the inferences drawn from UCE data are discussed more completely in Alda et al (2019).…”

“…The scale of data collection enabled by these approaches is unprecedented-a single researcher can collect sequence data from hundreds or thousands of loci across hundreds of taxa in a matter of weeks. The genome-wide distribution of these hundreds or thousands of loci can then be leveraged to: resolve relationships that were previously intractable (Alfaro et al, 2018), redefine our knowledge of the tempo of evolutionary change (Harrington et al, 2016), and help understand why relationships in some fish groups are so difficult to reconstruct (Alda et al, 2019).…”

The Multilocus Multispecies Coalescent: A Flexible New Model of Gene Family Evolution

“…With so many fully sequenced genomes/transcriptomes available, the proportion of one-to-one orthologs in typical multi-gene, multi-species data sets will become smaller and smaller, and most of the information about the history of genomes and organisms must be extracted from multi-copy gene families. This is particularly true of organisms having large, complex genomes and undergoing frequent hybridisation and large-scale duplications, such as the economically important angiosperms (Glémin et al, 2019;Stull et al, 2020) and fish (Alda et al, 2019;Campbell et al, 2020), to name just a few.…”