How to Make a Boy Shark
The reproductive organs of male chondrichthyans (sharks, rays, skates) are called claspers, paired structures that are inserted into the female to achieve internal fertilization. Claspers originate from the medial (inner) surfaces of the pectoral fins of male sharks, and immature claspers are present at birth/hatching. Little is known about the mechanisms that underlie clasper development in males, but not in females, though it has been thought that reproductive hormones must play a role in this sex-specific trait. Development of all organisms is controlled by gene expression - turning the right genes on and off at the appropriate times. In mammals and many other vertebrates we understand a great deal about the developmental processes that form the different body structures, and the genes that regulate these processes. Research into shark and ray development lags very far behind that of more commonly studied animals, but the formation of claspers is a process that can’t be studied in any of the popular research model organisms.
Now O’Shaughnessy et al have published a beautiful study examining the genes that regulate the development of claspers in the little skate, Leucoraja erinacea. They find that a gene called Sonic hedgehog (abbreviated Shh) is responsible for the development of claspers, and that male embryos keep expressing the Shh gene long after it has been turned off in humans. This is an exciting finding, as Shh is an important developmental gene in many other species up to an including humans. (The odd name of the gene comes from the appearance of Drosophila embryos lacking the gene, which have a spikey appearance resembling the video game hedgehog.) Despite its silly name, Shh is of major importance in development, involved in shaping everything from the fingers to the brain in humans.
O’Shaughnessy et al show that both male and female skate embryos initially express Shh during the development of the pelvic fins, but females turn off the gene after fin buds appear. In males, however, Shh expression remains active in the inner region of the pelvic fins, the tissue that will form the clasper (see figure). When they experimentally treated embryos with extra Shh the authors were able to induce the formation of small claspers even in female embryos! The question when studying gene expression, and finding that a particular gene is activated, is always well, what turns it on? For Shh expression in male skate pelvic fins, the authors show that it is the male hormones, called androgens, that keep Shh expression on. Even as an embryo, a male skate produces androgens, and these hormones maintain Shh, causing clasper development to begin. Female animals do not produce androgens, and so they silence Shh after pelvic fin development. This androgen control is not direct, however, the authors show that androgens turn on a different gene, called Hand2, and it is Hand2 expression that maintains Shh expression in male pelvic fins. This type of cascade is common in developmental biology, one gene activating another which activates another and another….
The paper is: O’Shaughnessy, Katherine L, Dahn, Randall D & Cohn, Martin J. Molecular development of chondrichthyan claspers and the evolution of copulatory organs. Nature Communications, DOI: 10.1038/ncomms7698.