Reproduction in Mesozoic birds and evolution of the modern avian reproductive mode

The reproductive biology of living birds differs dramatically from that of other extant vertebrates. Although some attributes of modern avian reproduction had their origin within theropod dinosaurs like oviraptors and troodontids, even the most derived non-avian theropods lack key features of modern birds. We review the current knowledge of reproduction in Mesozoic birds and 3 lines of evidence that contribute to our understanding of the evolution of the modern avian reproductive mode: (1) efforts to define the ancestral reproductive condition on the basis of extant birds, (2) the fossil record of non-avian theropod dinosaurs, and (3) the fossil record of reproduction in primitive Mesozoic birds (e.g., Enantiornithes). The fossil evidence from Mesozoic birds and non-avian theropods suggests that reproduction passed through 5 stages from basal theropods to neornithines: (1) pre-maniraptoran theropods, (2) oviraptor-grade maniraptorans, (3) troodontid-grade paravians, (4) Enantiornithes, and (5) basal Neornithes. Major changes occurred incrementally in egg size, shape, and microstructure; in nest form; in incubation method; and in parental care. Reproduction in troodontid theropods concurs with this clade representing the sister taxon to birds. Reproduction in enantiornithine birds included sequential ovulation from a single ovary and oviduct, eggs planted upright within sediments, and incubation by a combination of sediment and attendant adult or eggs fully buried with superprecocial young. Incubation modes of derived non-avian theropods and enantiornithines may have favored paternal care. Significant changes between enantiornithines and neornithines include an additional increase in relative egg size and sediment-free incubation. The latter permitted greater adult-egg contact and likely more efficient incubation. Associated changes also included improved egg shape, egg rotation, and chalazae-the albumin chords that suspend the yolk and facilitate proper embryonic development during rotation. Neornithes are the only Mesozoic clade of Dinosauria to nest completely free of sediment, and this may have played a crucial role in their surviving the K-Pg mass extinction event.