Reptilian Reproduction Functions with a Reduced Gonadotropin System

Vertebrate reproduction is controlled by two pituitary gondatropin hormones (GtHs), FSH and LH, binding to gonadotropin receptors (GtHRs) in gonadal tissues. All gnathostome vertebrates have been confirmed to possess at least one receptor for each gonadotropin hormone (LHR and FSHR), except for the reptiles, which showed inexplicable reactions to heterologous amphibian, avian, and mammalian GtHs in early endocrinological studies. This study investigated the number and function of reptilian GtHRs. Genomic and transcriptomic analyses of several selected tetrapod vertebrate species strongly suggested the inactivation of the LH receptor in all reptilian clades, a gene deletion that likely occured independently in the lepidosauria affecting the squamate reptiles and tuataras, and twice in the archelosauria clade, affecting testudines and crocodilia but sparing the avian class. Bioassays served to investigate the binding specificity of squamate, chelonian, crocodilian, avian, and mammalian GtHRs with their homo- and heterologous GtHs. The FSHR of a squamate lizard proved completely promiscuous to both its homologous GtHs, while the chelonian FSHR responded slightly stronger to the homologous LH than FSH, and the crocodilian FSHR was only stimulated by the homologous LH but not FSH. We therefore propose a modified paradigm with a neuroendocrine control of reproduction in reptilian species by only one GtHR and either one GtH in crocodilians and two GtHs in chelonians and squamate reptiles and discuss hypotheses of thightly regulated temporal and spatial expression of the remaining FSHR in different gonadal somatic cells and temperature-dependent functions of the only reptilian GtHR.