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Developmental gene expression as a phylogenetic data class: support for the monophyly of Arachnopulmonata

Abstract

Despite application of genome-scale datasets, the phylogenetic placement of scorpions within arachnids remains contentious between two different phylogenetic data classes. Paleontologists continue to recover scorpions in a basally branching position, partly owing to their morphological similarity to extinct marine orders like Eurypterida (sea scorpions). Phylogenomic datasets consistently recover scorpions in a derived position, as the sister group of Tetrapulmonata (a clade of arachnids that includes spiders). To adjudicate between these hypotheses using a rare genomic change (RGC), we leveraged the recent discovery of ancient paralogy in spiders and scorpions to assess phylogenetic placement. We identified homologs of four transcription factors required for appendage patterning (dachshund, homothorax, extradenticle, and optomotor blind) in arthropods that are known to be duplicated in spiders. Using genomic resources for a spider, a scorpion, and a harvestman, we conducted gene tree analyses and assayed expression patterns of scorpion gene duplicates. Here we show that scorpions, like spiders, retain two copies of all four transcription factors, whereas arachnid orders like mites and harvestmen bear a single copy. A survey of embryonic expression patterns of the scorpion paralogs closely matches those of their spider counterparts, with one paralog consistently retaining the putatively ancestral pattern found in the harvestman, as well as the mite, and/or other outgroups. These data comprise a rare genomic change in chelicerate phylogeny supporting the inference of a distal placement of scorpions. Beyond demonstrating the diagnostic power of developmental genetic data as a phylogenetic data class, a derived placement of scorpions within the arachnids, together with an array of stem-group Paleozoic scorpions that occupied marine habitats, effectively rules out a scenario of a single colonization of terrestrial habitat within Chelicerata, even in tree topologies contrived to recover the monophyly of Arachnida.

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Acknowledgments

We are indebted to Angelika Stollewerk and Matthias Pechmann for inviting this contribution. Russell Bicknell kindly provided a morphological data matrix for reanalysis. Melody Albright assisted with field collection of C. sculpturatus. Comments from Emily V.W. Setton, Guilherme Gainett, Jesús A. Ballesteros, and two anonymous reviewers improved a previous draft of the manuscript. Discussions with three colleagues in the paleontological community, Russell Garwood, Jason Dunlop, and Paul Selden, greatly refined some of the discussion on Paleozoic scorpions. James Lamsdell could not be reached for comment.

Funding

This work is based on material supported by National Science Foundation grant IOS-1552610 to PPS.

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Correspondence to Prashant P. Sharma.

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This article is part of the Special Issue “Crossroads in Spider Research—evolutionary, ecological, and economic significance”

Communicated by Matthias Pechmann

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Annotated multiple sequence alignments for all homologs and annotated tree files from phylogenetic analyses of three morphological datasets highlighted in Fig. 1 (TXT 36 kb).

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Nolan, E.D., Santibáñez-López, C.E. & Sharma, P.P. Developmental gene expression as a phylogenetic data class: support for the monophyly of Arachnopulmonata. Dev Genes Evol 230, 137–153 (2020). https://doi.org/10.1007/s00427-019-00644-6

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  • DOI: https://doi.org/10.1007/s00427-019-00644-6

Keywords

  • Arachnida
  • Rare genomic change
  • Arthropoda
  • Phylogenomics