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The earliest known vertebrate copulatory organs are claspers, paired penis-like structures that are associated with evolution of internal fertilization and viviparity in Devonian placoderms. Today, only male chondrichthyans possess claspers, which extend from posterior pelvic fins and function as intromittent organs. Here we report that clasper development from pelvic fins of male skates is controlled by hormonal regulation of the  Sonic hedgehog  ( Shh ) pathway. We show that Shh signalling is necessary for male clasper development and is sufficient to induce clasper cartilages in females. Androgen receptor (AR) controls the male-specific pattern of  Shh  in pelvic fins by regulation of  Hand2 . We identify an androgen response element (ARE) in the  Hand2  locus and present biochemical evidence that AR can directly bind the  Hand2  ARE. Together, our results suggest that the genetic circuit for appendage development evolved an androgen regulatory input, which prolonged signalling activity and drove clasper skeletogenesis in male fins.

Molecular development of chondrichthyan claspers and the evolution of copulatory organs