Superfoetative viviparity in a Carboniferous chondrichthyan and reproduction in early gnathostomes

Chondrichthyan fishes have an evolutionary history spanning over 400 million years and are characterized, in part, by internal fertilization. Traditionally, oviparity has been assumed to be the primitive birthing mode for these fishes and for vertebrates in general, with viviparity and matrotrophic nutrition being derived. The fossilized remains of two specimens of Harpagofututor volsellorhinus from the Upper Mississippian of Montana now provide the first direct evidence of matrotrophic live birth in a Palaeozoic chondrichthyan and of superfoetation in an extinct fish. Each female exhibits multiple foetuses of two size groups, indicating simultaneous gestation of multiple litters. There is no evidence of yolk sacs, only preserved organic pigments enveloping the young, suggesting matrotrophically derived material. Young were born large, as head lengths of the largest embryos measured up to 66 per cent of the mother's head length. Comparison of in utero embryos to isolated specimens suggests, unlike all extant chondrichthyans, the absence of a juvenile stage and rapid maturity. These new data suggest the advantages of superfoetative viviparity for a small bodied fish in a 318 Myr old species-and predator-rich marine bay. In the greater view of gnathostome evolution, this finding combines with other recent discoveries to document that multiple, and not necessarily closely related, species of both placoderms and chondrichthyans exhibited viviparity by the Upper Devonian and the Upper Mississippian. The capacity for internal fertilization probably predisposed members of these lineages to develop viviparity so early in gnathostome history. Yet, the surprising range of viviparity exhibited at this stage of vertebrate evolution emphasizes that derived reproductive strategies had evolved in gnathostomes by 380-318 million years ago. (C) 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 587-594.