Evolution of Placentation in Eugongylini (Squamata: Scincidae): Ontogeny of Extraembryonic Membranes in Oviparous and Viviparous Species of New Zealand

Abstract

New Zealand scincid lizards, genus Oligosoma, represent a monophyletic radiation of a clade, Eugongylini, of species distributed geographically throughout the South Pacific with major radiations in Australia and New Caledonia. Viviparity has evolved independently on multiple occasions within these lineages. Studies of Australian species have revealed that placental specializations resulting in substantial placentotrophy have evolved in two lineages. The pattern of extraembryonic membrane development of oviparous species differs from viviparous species and identical placental architecture has evolved in both placentotrophic lineages. We analyzed extraembryonic membrane development in two New Zealand species, the sole oviparous species, Oligosoma suteri, and placental development of a representative viviparous species, Oligosoma polychroma, using histological techniques. We conclude that these two species share a basic pattern of extraembryonic membrane development with other squamates. Comparisons with Australian species indicate that morphogenesis of the yolk sac of O. suteri results in an elaborate structure previously known only in Oligosoma lichenigerum with a geographic distribution on Lord Howe Island and Norfolk Island. This finding supports a close relationship between these two taxa. We conclude also that the pattern of placental development of O. polychroma is identical to that of viviparous species of Australia. The terminal placental stage for each of these lineages includes a chorioallantoic placenta and an elaborate omphaloplacenta. This level of homoplasy in placental evolution is consistent with a hypothesis that selection favors regional differentiation of the maternal–embryonic interface and that the omphaloplacenta is an adaptation for histotrophic transport.