House snake embryo at 6 days after oviposition (egglaying). The budding hemipenes can be seen at the caudal end of the embryo / Patrick Tschopp, PhD; Harvard Medical School, Department of Genetics
Janet Fang 05 Nov 2014, 21:56

Unlike humans and birds, male snakes and lizards have paired genitals. Called hemipenes, they’re almost like having two penises, but only one works at a time during sex. By studying mammal and reptile embryos, researchers have found a link between the evolution of external genitalia and the development of limbs. The findings, published in Nature this week, could help explain how vertebrates left the oceans for a life on the land. 

The shift to a terrestrial lifestyle required major adaptations in both locomotion systems and reproductive organs. The fin-to-limb transition has been studied a lot, but little is known about the origins of external genitalia. Previous studies have found similarities in the gene expression between limbs and genitals, but we don’t have an underlying mechanism to explain this link yet. 

To explore the connection, a team led by Harvard's Clifford Tabin examined embryos of a variety of land vertebrates, ranging from pythons and Anolis lizards to white leghorn chickens and lab mice. They found that, while there’s a lot of variation in the connection between limb and penis development in these animals, there’s a common mechanism that links the two processes. 

“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,” Tabin says in a news release. Hemipenes are made from the same tissue that hind limbs (or hind limb remnants in snakes) originate from. Mammal genitalia, on the other hand, are made from tail-bud tissue. So how do structures with the same function arise from such different starting material?  

The determining factor, they found, is the position of the cloaca—the opening for the reproductive, gut, and urinary tracts. (You can see lizard hemipenes and their cloacal opening here.) Where the cloaca is on the body helps organize development: The embryonic cloaca issues molecular signals that tell nearby cells and tissues to form into genitalia, and its location determines which tissues receive the signal first. 

In snakes and lizards, the cloaca is located closer to the tissue that also make a pair of legs. In mice, the cloaca is closer to the tail bud. A pair of legs, a paired penis; one tail, one penis. Here’s a python embryo 11 days after oviposition (or egglaying). The right hemipenis bud and vestigial limb-bud can be seen as two white blobs near the tail end of the embryo, at the center of the tail spiral.

To confirm that it’s all about location, location, location, the team grafted cloaca tissue next to the limb buds in one group of chicken embryos and beside the tail buds in another group. In both, cells close to the grafted cloaca responded to the signals and embarked on their genitalia fate. "By misplacing a molecular signal you can misguide these cells in their developmental trajectory," study author Patrick Tschopp of Harvard tells BBC.

Changes in the position of the “cloacal signaling center” during evolution leads to variation in the developmental route of external genitalia in animals. Tschopp adds: “An evolutionary shift in the source of a signal can result in a situation where functionally analogous structures are carved out of nonhomologous substrate."

In a related Scientific Reports study, a University of Florida duo identified the progenitor cells that contribute to the "genital tubercle," the precursor of the penis and clitoris. The genital tubercle arises from two populations of cells on the left and right side of the embryo, near the buds that give rise to the legs and the tail. Failure to fuse the left and right genital progenitor pools explains how snakes and lizards evolved paired penises.

Images: Patrick Tschopp, PhD; Harvard Medical School, Department of Genetics

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