When
it comes to genitalia, nature enjoys variety. Snakes and lizards have two.
Birds and people have one. And while the former group's paired structures are
located somewhat at the level of the limbs, ours, and the birds', appear a bit
further down. In fact, snake and lizard genitalia are derived from tissue that
gives rise to hind legs, while mammalian genitalia are derived from the tail
bud. But despite such noteworthy contrasts, these structures are functionally
analogous and express similar genes.
How
do these equivalent structures arise from different starting tissues?
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This
is a python embryo at 11 days after
oviposition (egglaying). The right
hemipenis
(genitalia) bud and vestigial limb-bud can be
seen near the tail end
of the embryo, in the
center of the tail 'spiral'. (two white 'blobs').
Photo Credit: Patrick
Tschopp.
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Reporting
in Nature, researchers in Harvard Medical School's Department of Genetics, led
by departmental chair Clifford Tabin, have found that the answer is not unlike
the real estate axiom Location, location, location.
The
embryonic cloaca -- which eventually develops into the urinary and gut tracts
-- issues molecular signals that tell neighboring cells and tissues to form
into external genitalia. The cloaca's location determines which tissues receive
the signal first. In snakes and lizards, the cloaca is located closer to the
lateral plate mesoderm, the same tissue that makes the paired limbs, receives
the signal. In mammals, the cloaca is closer to the tail bud.
To
further confirm this finding, the researchers grafted cloaca tissue next to the
limb buds in one group of chicken embryos, and beside the tail buds in a second
group. They found that in both cases, cells closer to the grafted cloaca
responded to the signals and partially converted toward a genitalia fate.
This
proves that different populations of cells with progenitor potential are able
to respond to cloaca signaling and contribute to genitalia outgrowth.
"While
mammal and reptile genitalia are not homologous in that they are derived from
different tissue, they do share a 'deep homology' in that they are derived from
the same genetic program and induced by the same ancestral set of molecular
signals," said Tabin, who is also the George Jacob and Jacqueline Hazel
Leder Professor of Genetics.
"Here
we see that an evolutionary shift in the source of a signal can result in a
situation where functionally analogous structures are carved out of
nonhomologous substrate," said Patrick Tschopp, an HMS research fellow in
genetics in Tabin's lab and first author on the paper. "Moreover, this
might help to explain why limbs and genitalia use such similar gene regulatory
programs during development."
Citation
Tschopp
P, Sherratt E, Sanger TJ, Groner AC, Aspiras AC, Hu JK, Pourquié O, Gros J, Tabin
CJ. A relative shift in cloacal location repositions external genitalia in
amniote evolution. Nature, 2014; DOI: 10.1038/nature13819