Devonian arthrodire embryos and the origin of internal fertilization in vertebrates

Evidence of reproductive biology is extremely rare in the fossil record. Recently the first known embryos were discovered within the Placodermi, an extinct class of armoured fish, indicating a viviparous mode of reproduction in a vertebrate group outside the crown-group Gnathostomata (Chondrichthyes and Osteichthyes). These embryos were found in ptyctodontids, a small group of placoderms phylogenetically basal to the largest group, the Arthrodira. Here we report the discovery of embryos in the Arthrodira inside specimens of Incisoscutum ritchiei from the Upper Devonian Gogo Formation of Western Australia (approximately 380 million years ago), providing the first evidence, to our knowledge, for reproduction using internal fertilization in this diverse group. We show that Incisoscutum and some phyllolepid arthrodires possessed pelvic girdles with long basipterygia that articulated distally with an additional cartilaginous element or series, as in chondrichthyans, indicating that the pelvic fin was used in copulation. As homology between similar pelvic girdle skeletal structures in ptyctodontids, arthrodires and chondrichthyans is difficult to reconcile in the light of current phylogenies of lower gnathostomes, we explain these similarities as being most likely due to convergence (homoplasy). These new finds confirm that reproduction by internal fertilization and viviparity was much more widespread in the earliest gnathostomes than had been previously appreciated.