Molecular development of chondrichthyan claspers and the evolution of copulatory organs

Katherine L. O’Shaughnessy,Martin J. Cohn,Randall D. Dahn

doi:10.1038/ncomms7698

Katherine L. O’Shaughnessy, Martin J. Cohn + Show 1 more

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https://doi.org/10.1038/ncomms7698

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Abstract

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.

Highlights

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
We investigate the molecular basis of clasper development in the little skate, Leucoraja erinacea, and show that Androgen receptor (AR) directly regulates Hand[2] to maintain Sonic hedgehog (Shh) signalling in pelvic fins of male embryos
The only skeletal structures posterior to the basipterygium are small nodular elements known as terminal cartilages (Fig. 1b,c; Supplementary Figs 1 and 2b)

Summary

Introduction

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. The origin of vertebrate copulation, internal fertilization and viviparity can be traced back B380 million years to the most basal gnathostome group, the placoderms[1,2,3] Fossils of these armored fishes show evidence of embryos internally, and adults have intromittent organs in the form of paired claspers that resemble those found in male chondrichthyans (sharks, skates, rays and chimaeras) but articulate at more posterior positions[1,2,3]. We investigate the molecular basis of clasper development in the little skate, Leucoraja erinacea, and show that AR directly regulates Hand[2] to maintain Shh signalling in pelvic fins of male embryos. This prolonged phase of Shh expression at the posterior margin of male pelvic fins sustains the appendage development circuit and promotes localized outgrowth of claspers

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