Confusion will be my epitaph: Genome-scale discordance stifles phylogenetic resolution of Holothuroidea

Abstract

Sea cucumbers (Holothuroidea) are a diverse clade of echinoderms found from intertidal waters to the bottom of the deepest trenches. Their reduced skeletons and limited number of phylogenetically-informative traits have long obfuscated morphological classifications. Sanger-sequenced molecular datasets have also failed to constrain the position of major lineages. Noteworthy, topological uncertainty has hindered a resolution for Neoholothuriida, a highly diverse clade of Permo-Triassic age. We perform the first phylogenomic analysis of Holothuroidea, combining existing datasets with twelve novel transcriptomes. Using a highly-curated dataset of 1,100 orthologues, our efforts recapitulate previous results, struggling to resolve interrelationships among neoholothuriid clades. Three approaches to phylogenetic reconstruction (concatenation under both site-homogeneous and site-heterogeneous models, and coalescent-aware inference) result in alternative resolutions, all of which are recovered with strong support, and across a range of datasets filtered for phylogenetic usefulness. We explore this intriguing result using gene-wise log-likelihood scores, and attempt to correlate these with a large set of gene properties. While presenting novel ways of exploring and visualizing support for alternative trees, we are unable to discover significant predictors of topological preference, and our efforts fail to favor one topology. Neoholothuriid genomes seem to retain an amalgam of signals derived from multiple phylogenetic histories.

Chronospaces: an R package for the statistical exploration of divergence times promotes the assessment of methodological sensitivity

“…This is in fact the expected behavior if topological incongruence is driven by biological factors such as ILS (Mendes & Hahn 2016). While some have argued that deep recalcitrant nodes are linked to ancient events of ILS (e.g., Cai et al 2021;Hime et al 2021;Mongiardino Koch et al 2023;Song et al 2023), it has also been suggested that topological incongruence at deep timescales is more likely to be . CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.…”

“…This is in fact the expected behavior if topological incongruence is driven by biological factors such as ILS (Mendes & Hahn 2016). While some have argued that deep recalcitrant nodes are linked to ancient events of ILS (e.g., Cai et al 2021;Hime et al 2021;Mongiardino Koch et al 2023;Song et al 2023), it has also been suggested that topological incongruence at deep timescales is more likely to be caused by methodological issues related to loss of signal and model inadequacy (Gatesy & Springer 2014;Richards et al 2018). While our analyses were not designed to test this phenomenon, our results are contrary to those expected if ILS was the main driver of topological conflict at ancient nodes.…”

Confusion will be my epitaph: genome-scale discordance stifles phylogenetic resolution of Holothuroidea

“…Raw files for all novel datasets, as well as those so far available only on EchinoDB [22], are deposited in the NCBI sequence read archive (SRA) under BioProject PRJNA979278. All assemblies are available at the associated Dryad data repository (doi:10.5061/dryad.0p2ngf255) [26], along with the phylogenetic matrices, trees and other results derived from them.…”

“…COI sequences are available from GenBank under accession numbers OR082743-OR082756 and OR145350-OR145353; transcriptomic raw reads are available from SRA under BioProject PRJNA979278. All assemblies, phylogenomic datasets and trees, and other results, can be obtained from the Dryad Digital Repository: https://doi.org/10.5061/dryad.0p2ngf255 [26].…”

Larval development in the apodid sea cucumber Chiridota gigas, with a focus on coelom development and the serotonergic nervous system during metamorphosis

“…The order Apodida is a basal group in the class Holothuroidea, as shown in both morphological and molecular analyses (Kerr & Kim, 1999Lacey et al, 2005;Miller et al, 2017;Mongiardino Koch et al, 2023;Sun et al, 2021). Within the families Chiridotidae and Synaptidae, there is a diversity of developmental types: planktotrophic auricularia, lecithotrophic doliolaria, and coelomic and intraovarian brooding (Clark, 1908;Sewell et al, 2024;Smiley et al, 1991).…”