When two become one: the evolution and development of external genitalia on land

By Mara Laslo

When our ancestors first crawled onto land, they faced some serious challenges. How could they support and move their body weight outside of the water? How could they breathe? Perhaps most importantly, how could they reproduce without water? Our early ancestors probably reproduced in water much like most amphibians do today, by releasing sperm to swim to nearby eggs. Laying eggs on land, however, carries a significant risk of drying out, or desiccation. The evolution of an amniotic sac that surrounds and protects the embryo during development prevents desiccation, but also creates a barrier to sperm. That means for amniotes, fertilization has to occur prior to enclosing the embryo in the protective casing—it has to be internal. This is where intromittent organs come in.

Intromittent organs, like the mammalian penis and snake hemipenes (see below), are important adaptations that allow amniotes to be successful land dwellers. How did these organs evolve? We can’t travel back in time to watch it happen, but studying how diverse amniotic external genitalia develop in species alive today can help us understand how this important transition happened in our own evolutionary past.



Neil Shubin discusses the challenges our ancestors faced when they transitioned from water to land.


Because most amphibians fertilize their eggs in water, but live part of their lives on land, they often serve as an approximation of our first land-dwelling ancestors. Both male and female amphibians have a cloaca, an opening that releases the sperm and egg during mating. This structure is also present in mammal and reptile embryos, but as development progresses, molecular signals from the embryonic cloaca tell the surrounding tissue to grow and differentiate into external genitalia. In Nature’s November 2014 issue, Tschopp et al. (2014) describe how merely changing the position of this signaling center could result in the diversity of amniotic genitalia.

Squamates, like the anole lizard, have complex forked external genitalia called hemipenes. The hemipenes are located near the limbs and develop from the same population of embryonic cells. Mammalian genitalia are located closer to the tail, and arise from the same cells that later produce the tail.

Reproduced with author’s permission (http://www.reptilescanada.com/archive/index.php/t-44116.html)

Using high-throughput sequencing techniques, researchers gain a broad picture of the genes and gene regulatory networks (basically a molecular signature) involved in forming a specific tissue. It turns out that the molecular signatures of the developing mouse limb and genitals are very different from the start. In contrast, the molecular signatures found in the developing genitalia and limbs of the anole lizard are quite similar and don’t show many differences until later in development, reflecting their common developmental origin. Some even speculate that this shared developmental pathway with limbs may be why squamates have two hemipenes and mammals only have one penis.

On the molecular level, lizard genitalia and limbs are far more similar to each other than mice genitalia and limbs, and this reflects their developmental origins in different tissues. Tschopp et al. hypothesize that genitalia origins differ because the signaling center, the cloaca, is in a different relative position. Both chicken and quail reproduce using something called the “cloacal kiss”—basically just mushing their cloacas together. We know that these birds lost their external genitalia rather recently because some birds still do have penises (ducks & ostriches) and their closest evolutionary relative, reptiles, also still have external genitalia. This makes these birds perfect for Tschopp and colleague’s experiments; it’s likely that each bird will still respond to signals from the other’s cloaca to produce genitalia. Moving the cloaca signaling center from a chicken to a quail’s tail bud area causes outgrowths that have the same molecular signature as external genitalia. This demonstrates that the cell population in the tail is competent, meaning able to respond, to the signals coming from the developing cloaca. Shifting the cloaca closer to the tail bud could result in external genitalia developing from this tissue. This re-use of common mechanism, or signaling center, is a common theme in developmental biology. For example, turtles have a unique body plan—but their shell is formed using a signaling center that also has a large role in limb development (Gilbert et al. 2001; Nagashima et al. 2007).

Figure 2. Determining which part of the embryo becomes the genitalia. Labeling early limb cells (green) in the mouse and tracking the labeled cells over development shows the label in the limbs, but not the genitalia (a, b). After labeling the mouse tail bud, however, labeled cells are found in the genitalia (c). Two cell populations develop into the genitals in chickens (d, e, f), whether the early limb or tail bud is labeled. Labeling the anole early limb cells labels both the hemipenes and the limb (g, h), while after labeling only the tail bud, there are no labeled cells in the hemipenes.

Figure 2. Determining which part of the embryo becomes the genitalia. Labeling early limb cells (green) in the mouse and tracking the labeled cells over development shows the label in the limbs, but not the genitalia (a, b). After labeling the mouse tail bud, however, labeled cells are found in the genitalia (c). Two cell populations develop into the genitals in chickens (d, e, f), whether the early limb or tail bud is labeled. Labeling the anole early limb cells labels both the hemipenes and the limb (g, h), while after labeling only the tail bud, there are no labeled cells in the hemipenes.

Tschopp et al. are notable for their combination of classical developmental biology techniques, such as grafting (moving the developing cloaca to somewhere else in the body) and modern high-throughput sequencing. Together, the data suggest a co-option, or a repurposing, of a limb-like structure for reproductive purposes sometime in our evolutionary history. While it is fun to speculate about what our ancestors looked like, it’s most reasonable to conclude that our ancestors used the same developmental genes for limb and genitalia development and that shifts in the cloaca signaling center may explain some of diversity of amniotic external genitalia. The “deep homology”, or molecular similarity, of limbs and genitalia is a compelling part of studying evolutionary and developmental biology—we constantly discover that, under the skin, we have more in common with diverse life forms than we think.

Mara Laslo is a PhD candidate in the Department of Organismic and Evolutionary Biology at Harvard University.

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