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

Title
A relative shift in cloacal location repositions external genitalia in amniote evolution
Publication Date
2014
Author(s)
Tschopp, Patrick
Sherratt, Emma
Sanger, Thomas J
Groner, Anna C
Aspiras, Ariel C
Hu, Jimmy K
Pourquie, Olivier
Gros, Jerome
Tabin, Clifford J
Type of document
Journal Article
Language
en
Entity Type
Publication
Publisher
Nature Publishing Group
Place of publication
United Kingdom
DOI
10.1038/nature13819
UNE publication id
une:17403
Abstract
The move of vertebrates to a terrestrial lifestyle required major adaptations in their locomotory apparatus and reproductive organs. While the fin-to-limb transition has received considerable attention, 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 genitals; however,no underlying developmental mechanism has been identified. We re-examined this question using micro-computed tomography, lineage tracing in three amniote clades, and RNA-sequencing-based transcriptional profiling. Here we show that 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 hind limbs, 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 cloaca demonstrates 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 limb molecular circuitry owing to a common evolutionary origin.
Link
Citation
Nature, 516(7531), p. 391-394
ISSN
1476-4687
0028-0836
Start page
391
End page
394

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