A relative shift in cloacal location repositions external genitalia in amniote evolution

Patrick Tschopp, Emma Sherratt, Thomas J. Sanger, Anna C. Groner, Ariel C. Aspiras, Jimmy K. Hu, Olivier Pourquié, Jérôme Gros, Clifford J. Tabin*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Themove of vertebrates to a terrestrial lifestyle requiredmajor adaptations intheir locomotory apparatus and reproductive organs.While the fin-to-limb transition has received considerable attention1,2, little is known about the developmental and evolutionary origins of external genitalia. Similarities in gene expression have been interpreted as a potential evolutionary link between the limb and genitals3-6; however,nounderlying developmentalmechanismhas been identified. We re-examined this question using micro-computed tomography, lineage tracing in threeamniote clades, andRNA-sequencing-based transcriptional profiling. Here we showthat the developmental origin of external genitalia has shifted through evolution, and in some taxa limbs and genitals share a common primordium. In squamates, the genitalia develop directly from the budding hindlimbs, or the remnants thereof, whereas in mice the genital tubercle originates from the ventral and tail bud mesenchyme. The recruitment of different cell populations for genital outgrowth follows a change in the relative position of the cloaca, the genitalia organizing centre. Ectopic grafting of the cloacademonstrates the conserved ability of different mesenchymal cells to respond to these genitalia-inducing signals.Our results support a limb-like developmental origin of external genitalia as the ancestral condition.Moreover, they suggest that a change in the relative position of the cloacal signalling centre during evolution has led to an altered developmental route for external genitalia in mammals, while preserving parts of the ancestral limbmolecular circuitry owing to a common evolutionary origin.

Original languageEnglish
Pages (from-to)391-394
Number of pages4
JournalNature
Volume516
Issue number7531
DOIs
Publication statusPublished - 18 Dec 2014
Externally publishedYes

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