Non-Avian Reptile Reproduction Functions with a Reduced Gonadotropin System

Vertebrate reproduction is controlled by two pituitary gonadotropin 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 GtH (LHR and FSHR), except for species of the reptilian (non-avian sauropsidan) orders, such as lepidosauria, testudines, and crocodylia, 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 selected tetrapod species now strongly suggest the inactivation of the LH receptor in all non-avian sauropsidans. This gene inactivation likely occurred independently in three branches of the sauropdisan clade, sparing only the avian class. Bioassays served to investigate the binding specificity of squamate, chelonian, crocodilian, avian, and mammalian GtHRs with their homologous 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 crocodylian FSHR was only stimulated by the homologous LH but not FSH. We therefore propose a modified paradigm with a neuroendocrine control of non-avian reptilian reproduction by a single GtHR and either one GtH in crocodylians or two GtHs in chelonians and squamate reptiles. Finally, we discuss hypotheses of tightly regulated temporal and spatial expression of the remaining FSHR in different gonadal somatic cells and temperature-dependent functions of the single non-avian reptilian GtHR.