Vestigial organs alter fossil placements in an ancient group of terrestrial chelicerates

Guilherme Gainett*, Benjamin C. Klementz, Pola Blaszczyk, Emily V.W. Setton, Gabriel P. Murayama, Rodrigo Willemart, Efrat Gavish-Regev, Prashant P. Sharma

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Vestigial organs provide a link between ancient and modern traits and therefore have great potential to resolve the phylogeny of contentious fossils that bear features not seen in extant species. Here we show that extant daddy-longlegs (Arachnida, Opiliones), a group once thought to possess only one pair of eyes, in fact additionally retain a pair of vestigial median eyes and a pair of vestigial lateral eyes. Neuroanatomical gene expression surveys of eye-patterning transcription factors, opsins, and other structural proteins in the daddy-longlegs Phalangium opilio show that the vestigial median and lateral eyes innervate regions of the brain positionally homologous to the median and lateral eye neuropils, respectively, of chelicerate groups like spiders and horseshoe crabs. Gene silencing of eyes absent shows that the vestigial eyes are under the control of the retinal determination gene network. Gene silencing of dachshund disrupts the lateral eyes, but not the median eyes, paralleling loss-of-function phenotypes in insect models. The existence of lateral eyes in extant daddy-longlegs bears upon the placement of the oldest harvestmen fossils, a putative stem group that possessed both a pair of median eyes and a pair of lateral eyes. Phylogenetic analysis of harvestman relationships with an updated understanding of lateral eye incidence resolved the four-eyed fossil group as a member of the extant daddy-longlegs suborder, which in turn resulted in older estimated ages of harvestman diversification. This work underscores that developmental vestiges in extant taxa can influence our understanding of character evolution, placement of fossils, and inference of divergence times.

Original languageAmerican English
JournalCurrent Biology
DOIs
StatePublished - 25 Mar 2024

Bibliographical note

Publisher Copyright:
© 2024 Elsevier Inc.

Keywords

  • arrestin
  • Bayesian node-dating
  • Chelicerata
  • ocelli
  • Pax2
  • Pax6
  • phylogeny
  • RDGN
  • rudimentary organs
  • sine oculis

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