Why did the chicken cross the road? Maybe it was looking for its penis.

Science Sushi
By Christie Wilcox
Jun 6, 2013 8:00 PMNov 20, 2019 2:41 AM

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Warning: the following may be considered NSFW, particularly if your employer finds avian genitalia inappropriate.  Thanks to the detailed research of Patricia Brennan and the fluent coverage of it by Ed Yong and Carl Zimmer, a lot of people have not only heard of the impressive duck penis, they've seen it in all its explosive glory (if you don't know what I'm talking about, take a moment to click on the links above — trust me, it's worth it).

Why do chickens and other birds lack the fancy phalluses of their relatives? Good question. At least, now, we know how...Image from Herrera et al., Fig 1. But while ducks and their fellow water fowl boast these impressive, large penises, the penes of most birds are nothing to squawk about. Ninety-seven percent — over 10,000 species of birds — have either reduced or non-existant penises that are incapable of penetration. "One of the most puzzling events in evolution is the reduction and loss of the phallus in birds," explains biologist Marty Cohn in a Cell Press Video Abstract. "It's remarkable that a group of animals would eliminate a structure that is so important for reproduction." Given that, like us, birds conceive through internal fertilization, you would think a penis would be essential. How else is the male's sperm supposed to get all up in the female's vagina? While scientists still debate about why the chicken lost most of its penis, a new study published this week in Current Biology finally explains how it was lost, a crucial first step in unraveling this evolutionary enigma.

Chick porn: a developing chicken's penis (red) before it regresses, visualized by a scanning electron microscope.Image c/o A.M. Herrera and M.J. Cohn, University of Florida Marty Cohn and his lab at the University of Florida study the development and evolution of appendages, and are particularly interested in the bird penis conundrum. "It really catches your attention when you see a species that reproduces by internal fertilization and realize that it lacks a penis, which we tend to think of as a critical organ for this mode of reproduction," explains lead author of the study and Cohn's graduate student Ana Herrera. To get to the bottom of mystery of avian penises, Herrera and fellow grad student Claire Perriton, with the aid of undergrad Simone Shuster, watched developing bird embryos closely to see exactly when and how the development of genitalia in the micropenis-wielding chickens diverges from that of their well-endowed duck cousins. They found that through the first stages of development, the two embryos grow the same way. Male chickens begin life with a normally-forming penis. But then, as development progresses, everything changes. In chickens, the penis stops growing and even shrinks, while the duck penis continues to extend and extend, eventually coiling. When the team began examining these developmental penises at the cellular level, they expected that the cessation of growth by the chicken's penis would be due to a decrease in cell division — but it wasn't. "We expected to find that some critical outgrowth factor was missing," said Cohn. Instead, the proliferation pathways in developing duck and chicken penises were the same, even after the stage when the chicken penis starts to regress. Since the signal for penis enlargement is steady throughout, the team realized that developmental penis growth has to be controlled instead by cell death.

LysoTracker Red staining shows widespread apoptosis (cell death) in the tip chicken and quail developing penises, whereas duck, goose, emu, and alligator genitalia at comparable stages show limited death. The brighter the orange, the more death is occurring. Image from Herrera et al., Fig. 3. What we consider growth is really the delicate balance between two opposing cellular processes: proliferation and death. When cells divide more than they die, parts grow; when the die more than they divide, those parts shrink. Since the developmental chicken penises were proliferating at the same rate as duck penises, the team instead looked at the rate of programmed cell death, called apoptosis. Sure enough, the developing penises of chickens and penis-less birds showed increased death at the tip, while the forming penises of the phallus-retaining duck, emu and alligator showed much less apoptosis. They then went a step further, tying the death to the expression of a gene called BMP4, a part of the bone morphogenetic protein (BMP) pathway well known for its role in apoptosis. When they blocked BMP4 expression in developing chicks, their penises continued to grow; when they induced it in ducks, penis growth halted. "It was surprising to learn that genital outgrowth fails in these birds not due to absence of a critical growth factor, but due to presence of a cell death factor," said Herrera. Cohn and Herrera were quick to point out that understanding bird genitalia has much broader implications. Reproductive organs evolve extremely quickly and are affected by more birth defects than almost any other organ. "Despite the high incidence of birth defects affecting the genitalia, genital development is not well understood at the molecular genetic level," explains Cohn. By understanding the developmental variation in animals like birds, Cohn hopes to shed light on developmental discrepancies in a wide variety of animals, including us. "This [research] allows us to understand not only how evolution works, but also to gain new insights into possible causes of malformations." Perhaps what's most interesting about this discovery is that it means chickens and other galliform birds likely haven't lost the ability to create a full penis. Instead, a novel anti-penis pathway counteracts extension early on. If, though, that pathway were to be disrupted by a new evolutionary event, the penes would grow. This might explain why chachalacas, guans and curassow — birds in the family Cracidae — possess penetrative penises. They alone in the entire lineage of Galliformes boast these appendages, and the team thinks that this unique group didn't keep their penises throughout evolutionary history, they got them back. "In light of current phylogeny, cracids may have re-evolved an intromittent phallus," write the authors. "which would suggest that galliforms have retained the competence to redevelop a phallus from a rudimentary genital organ." Which, of course, still leaves scientists wondering why Galliformes lost their penises in the first place. Some have suggested that the reduction of the galliform penis occurred as an evolutionary accident or side-effect of sorts — a phenomenon biologists call pleiotropy. Pleiotropy occurs because individual genes are involved a suite of traits in different parts of the body, thus a mutation in a single gene can cause changes in two otherwise unrelated observable traits. If one of these trait changes is strongly beneficial, both changes might stick around, even if the other is less than ideal. When it comes to birds and penises, we know (thanks especially to the work of Cohn and Herrera) that the molecular mechanisms that control development aren't unique to genetalia. The same gene networks also control the formation of the limbs, gut, nervous system, muscle, and even feathers. It's possible, then, that the shift in development of any of these traits could have altered penile development. Many scientists find the idea that the penis could be so 'accidentally' lost unlikely, though. The reduction of such an important appendage could not have easily been outweighed by benefits to other areas, they argue, thus selection on the penis itself would have had to come into play at some point, at least in a stabilizing manner. In other words, the reduced phallus had to have been a little advantageous. Many alternative hypotheses have been suggested as to what selective pressures pushed for penis loss in Galliformes, from the flying cost of a heavy member to the lack of need for deep penetration outside of aquatic environments, but the strongest center around the idea of female choice. For fertilization to occur in the absence of a penis, females have to cooperate with their would-be mates. In most birds, the female must present her cloaca and evert her vagina before the male can inseminate her. Such behavior gives the females total control over the literal act of sex as well as paternity. Unlike male ducks, male chickens can't rape their partners or force copulation; they have to convince the female they're worth the effort, or they don't get any. Period. This fact alone suggests that sexual selection may be to blame for the tiny penes, and suggests that early female Galliformes preferred to mate with poorly-hung males — whether the ultimate reason for that was to affirm mate choice, prevent rape, avoid STDs, or even get things over with quickly to avoid predation. Now that we know the molecular details of how the Galliformes lost their members, scientists can begin to whittle away at the different options and attempt to figure out which hypothesis fits best. For now, Cohn and Herrera are leaving that debate to evolutionary biologists and ecologists. "We study embryonic development in a wide range of species," said Herrera. "While asking why this happened is a fascinating question, as developmental biologists, we were interested in discovering how this change occurred" — and, discover they did. From the developmental perspective, the case of the missing avian penes is closed. "Whatever the evolutionary forces that drove this change, our finding shows that, at the genetic level, it resulted in a change in the regulation of BMP4 expression, which causes the embryonic phallus to regress due to programmed cell death."

Citation: Herrera A., Shuster S., Perriton C. & Cohn M. (2013). Developmental Basis of Phallus Reduction During Bird Evolution, Current Biology, 23 1-10. DOI: 10.1016/j.cub.2013.04.062

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