Ever
seen a pair of pigeons going at it? And
did you notice a penis on the male pigeon?
The answer is no, because most birds do not have external genitalia
large enough for penetration. And yet
birds reproduce via internal fertilization.
Why would evolution favor male genitalia too small to actually enter
into the female? This just seems so
inefficient.
There
are a few birds that do have well developed phalluses, such as the duck and
goose. What happened during evolution
that caused some birds to retain a phallus, whereas most other birds lost
it? A paper appeared this week in
Current Biology by Herrera et al., which addresses these questions from a
developmental point of view.
Developmental
arrest
The
authors started this study by comparing the development of the phallus in
embryos of two different birds. They
chose to look at (1) chick embryos, which are part of the galliformes group of
birds and have reduced phalluses and (2) duck embryos, which are part of the
anseriforms group, which have well developed, penetrating penises. They followed the growth of the genital
tubercle, the tissue that will form the penis.
As the duck and chick embryos grow, so do their genital tubercles, with
no noticeable difference between the two species during the early stages of
development. At a later time period,
though, the tubercle stops growing and regresses in the chicks, while the duck
keeps on growing. This shows that the
tissue that makes the two different types of phalluses has the same
developmental origin.
Why
does the genital tubercle stop growing in the chick?
From
a molecular stand point, the chick embryos could either lose the “growth”
signal or they could gain expression of a “stop” signal not present in ducks. From work in other animals, the authors knew
that there are two major growth signals responsible for guiding the development
of the external genitalia – Sonic Hedgehog (Shh) [see my other post about this protein] and Hox13. These two genes are
strongly expressed in the duck genital tubercle throughout embryonic
development, as expected. Surprisingly,
though, they are also strongly expressed in the chick embryos. This means that the chickens haven’t lost the
growth signal.
The
authors then investigated if there is some sort of a “stop” signal in the
chicks. They found that in chicks and
quails, with reduced phalluses, there is a lot of cell death in the genital
tubercle in the later stages of development.
This could account for the regression of the genital tubercle. They then found that the chicks highly
express a protein called BMP4 at the tip of the tubercle, which induces cell
death, whereas ducks do not.
In
fact, by overexpressing BMPs in the duck, they induced cell death in the genital
tubercle. In the opposite experiment, they
inhibited BMPs in the chick and their genital tubercles increased growth, as if
they were ducks.
In
summary:
Chicken: + BMP --> increased cell death --> reduced phallus
Duck: - BMP --> no cell death, so
continued tissue development --> large phallus
Evolution
of reduced phallus
So
what does this mean? Chicks and quails
have reduced phalluses, because during development, they express BMP4, which
tells the developing cells of the penis to die off. One really cool thing that the authors did
next was to look at cell death in the closest relative to birds-- the
alligator. Yah, they got alligator
embryos for this research! Alligators
have developed phalluses and they show hardly any cell death in the genital
tubercle. From this work, they could
create an evolutionary tree, which shows that chicks and quails most likely evolved
the BMP4 signal after their group separated from ducks. Although the authors didn’t test any members
(ha ha) from the neoaves group, which includes most other birds, we can presume
that they also have a similar cell death mechanism to reduce the development of
their phalluses.
 |
| Phylogenetic tree of birds, showing when the BMP signal evolved. (Adapted from Herrera et al., 2013) |
This
still begs the question of why would natural selection favor a reduced phallus
so much so that it evolved independently in different lineages? The authors propose two different theories,
both of which may have occurred:
1)
Sexual selection – sure, it may not be favorable for the males to have reduced
phalluses, but it might be advantageous for the females. In order for insemination to occur in these
species, the female has to be a willing participant to allow the male to shimmy
up next to her and release the sperm in very close proximity. This gives the females the power to select
their mates. As opposed to species with
large penises, where the male could basically rape the female and still
successfully pass on his genes to the next generation.
2)
Pleiotropy – this term refers to when a single gene mutation can lead to
multiple noticeable changes in the body.
BMPs are a major signal during development of animals. BMPs are involved in a number of bird-only
innovations such as feathers and beaks.
Maybe increased BMP expression gave an advantage to these birds, but
also lead to reduced phalluses, as a secondary effect. This may have occurred first in evolution,
but sexual selection may have stabilized this characteristic in the population.
This
article was so clear and interesting.
I’m sure it will catch people’s attention because of the subject matter,
but it’s a great example of using development to solve an evolutionary
question. Plus it gives reviewers and
bloggers a great opportunity to think up clever titles and puns for their
articles. The review that was published
alongside this article was titled “Cock-a-doodle-don’t”. How can I compete with that?
