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

“…with asymmetrical flight feathers but lacking a keeled sternum and triosseal canal, the osteological correlates of the modern flight stroke (Ostrom 1976, Nudds and Dyke 2010); nor strongly ornamented eggs with a largely avian microstructure as in oviraptors (Grellet-Tinner et al. 2006).”

“…respiratory system, brain, feathered integument, and even small body size with Neornithes (Larsson et al. 2000, O’Connor and Claessens 2005, Prum 2005, Turner et al. 2007) and that Mesozoic birds are largely indistinguishable from their closest relatives in morphospace (Brusatte et al. 2014).”

“However, after several morphometric investigations (Chiappe et al. 2008, 2010, Peters and Peters 2009, 2010, Marugán-Lobón et al. 2011), the dimorphism remains unclear; interpretations include one species with sexes differing in the presence of rectrices (Feduccia 1996, Chiappe et al. 1999,…”

“Although a multitude of factors undoubtedly influenced avian evolution at the end-Cretaceous mass extinction, including diet [24, 28], body size [19], breeding habits [27], and flight capacity [53], selection for non-arboreal habits appears to have left an indelible mark on the early evolutionary history of crown bird…”

“For these reasons, it seems likely that the possibility of ‘tight sitting’ is weaker in oviraptorid maniraptorans than troodontids (a more probable contact incubator; Varricchio et al. 2013, 2018; Tanaka et al. 2015; Varricchio & Jackson 2016).”

“, 2020), including aspects of reproductive biology (Zelenitsky and Therrien, 2008; Varricchio and Jackson, 2016; Norell et al., 1995; Varricchio et al., 2002).”

“All evidence thus far indicates the Enantiornithes were highly precocial, often described as superprecocial [35,36].”

“Conclusions Varricchio and Jackson (2016) suggested that oviraptorgrade maniraptorans represent one of five evolutionary stages of reproduction from basal theropod dinosaurs to neornithines.”

“…behavioural and reproductive traits corroborate close avian affinities for troodontids (Xu & Norell 2004; Varricchio & Jackson 2004; Gao et al. 2012; Varricchio & Jackson 2016), and troodontid digestive processes may also be closer to avian conditions than other coelurosaurs (Zanno & Makovicky…”

“C), a feature also known in modern and fossil crocodyliform eggshells (see Hirsch and Quinn, 1990; Tanaka et al., 2011; Moreno-Azanza et al., 2014a, 2015; Marzola et al., 2015, Table 3; Srivastava et al., 2015; Jackson and Varricchio, 2016; Russo et al., 2017).”

“Birds also possess this trait, but they generally produce fewer, relatively large eggs (10) that are formed iteratively (rather than “en masse”) via a single ovary-oviduct system (11).”

“FOSS I L eggs and eggshells provide a unique opportunity to study aspects of the reproductive biology of extinct amniotes (e.g. Tanaka et al. 2015, 2019; Varricchio & Jackson 2016; Amiot et al. 2017; Wiemann et al. 2018; Choi et al. 2019a).”

“The fossil evidence suggests that dinosaurs within the clade Pennaraptora began to lay their eggs closer to ground level so the eggs were partially exposed thereby representing an important shift in nest sites by the avian ancestors [10,33].”

“It is therefore likely that egg deposition in soil is primitive for birds, and it has been supposed that nesting free of sediment is a derived characteristic, which evolved within Ornithuromorpha (Varricchio and Barta 2015; Varricchio and Jackson 2016).”

“Extant amniotic eggs are traditionally classified into soft-shelled, leathery and hard-shelled ones [ 45 , 50 –52 ] (see Supplementary Data ), though this classification oversimplifies the great variety of eggshell morphologies [ 4 8 ].”

“In combination with the hypothesis that oviraptorids were communal nesters and the male was in charge of incubating the whole clutch (Varricchio et al. 2008; Moore and Varricchio 2016), the male may have started incubation before several females completed the clutch.”

“…incrementally through generations (Lorenz 1958; Gould 1982; Gomez and Miikkulainen 1997), then an ancestor of modern birds likely did use partialburial nesting strategies (as ancestral reptiles used subterranean nests and modern birds tend to build subaerial ones) (Varricchio and Jackson 2016).”

“The Spooner Egg is notably broad for its length [63], which may indicate it was laid by a megapode with an especially large pelvis [66], given that egg size in birds is constrained by pelvis size [69].”

“Egg asymmetry is only pronounced among troodontids, and eggshell microstructure becomes increasingly avian-like as well [8].”

“…that the parental care of troodontids and oviraptorosaurs (both maniraptoran dinosaurs) are akin to the reproductive strategies of palaeognath birds with males incubating eggs from several females and taking care of the young after hatching (Varricchio et al., 2008; Varricchio & Jackson, 2016).”

“…the following: sequential ovulation; eggshells with avian features; asymmetric eggs; iterative egg-laying; parental brooding; paternal care; and hatching asynchrony (Varricchio & Jackson, 2016; Varricchio et al., 2008; Yang et al., 2019; but see Birchard, Ruta, & Deeming, 2013; Deeming, 2015).”

“The latter is supported by various lines of evidence including the presence of a cuticle layer [59], and eggshell conductance (which depends on eggshell porosity) which is lower in oviraptor (and troodontid) eggs than in other non-avian dinosaurs [41,45,60].”

“Although these constraints are not well understood outside of crown birds (Varricchio and Jackson 2016), this may explain why paravians in our sample present a more significant relationship between eggshell thickness and egg mass, and a decrease in variance for relative eggshell thickness (Fig.”

“In addition, the eggs of M. ganzhouensis are arranged randomly in the clutch, rather than vertically oriented prismatoolithid eggs (Zelenitsky and Hills 1996; Varricchio and Jackson 2016).”

“However, Elzanowski (1981) and Varricchio and Jackson (2016) recognize the existence of fusion in some of the thoracic vertebrae in enantiornithine embryos from the Upper Cretaceous of Mongolia, which could be a notarium precursor.”

“Notably, ovirap-torosaurs appear to have had larger clutch volumes than are predicted for their body mass (Varricchio and Jackson 2003, 2016), and perhaps their unique nesting mode aided successful incubation of their proportionally large clutches.”

“Moreover, greater taphonomic understanding may help clarify the nesting behaviours and reproductive physiology of non-avian theropods and ancient birds such as enantiornithines (Horner et al. 1994; Hayward et al. 2000, 2011; Varricchio and Jackson 2016).”

“In extant sexually dimorphic bird species with open nests, though the male may be ornamented, females, which more often brood and tend to the nest, typically have cryptic plumages to reduce the risk of predation to both themselves and their young [69,85-90].”

“For analyses within the crown, these results fit 169 within this theory – that a limited number of avian lineages were able to survive the end-Cretaceous 170 mass extinction, possibly due to factors such as their incubation mode [31], followed by explosive 171 diversification in the Cenozoic likely aided by the remova…”

“Of special importance to this issue are how the dinosaurs dwelling on arctic Franklinia (Russell 1990; Vavrek et al. 2014) when it was separated from the rest of Appalachia were outright blocked from migrating below the paleo arctic circle by the Hudson Seaway (Fig.”

“Many other avialan reproductive traits had non-avialan theropod origins, at minimum, including hatching asynchrony 138–140 , monoautochronic ovulation (paired ovaries each releasing one egg simultaneously) 141 , and three-layered eggshell microstructure 142,143 and egg pigmentation 144 .”

“In this context, they may have nested on the ground — consistent with the widespread ground-nesting habit inferred for non-avian dinosaurs and many early birds 56,57,75,76 — while retaining greater dispersal potential than modern fl ightless forms.”

“There is usually no evidence of egg pairs (but see Varricchio et al., 2002 for eggs with paired pattern) and the eggs are nearly perpendicularly laid on the ground with their blunt end upward and lower half buried (Varricchio & Jackson, 2016; Zhao, 2003).”