An Early Cretaceous enantiornithine (Aves) preserving an unlaid egg and probable medullary bone

Abstract

Understanding non-crown dinosaur reproduction is hindered by a paucity of directly associated adults with reproductive traces. Here we describe a new enantiornithine, Avimaia schweitzerae gen. et sp. nov., from the Lower Cretaceous Xiagou Formation with an unlaid egg two-dimensionally preserved within the abdominothoracic cavity. Ground-sections reveal abnormal eggshell proportions, and multiple eggshell layers best interpreted as a multi-layered egg resulting from prolonged oviductal retention. Fragments of the shell membrane and cuticle are both preserved. SEM reveals that the cuticle consists of nanostructures resembling those found in neornithine eggs adapted for infection-prone environments, which are hypothesized to represent the ancestral avian condition. The femur preserves small amounts of probable medullary bone, a tissue found today only in reproductively active female birds. To our knowledge, no other occurrence of Mesozoic medullary bone is associated with indications of reproductive activity, such as a preserved egg, making our identification unique, and strongly supported.

Dinosaur paleohistology: review, trends and new avenues of investigation

“…Since this first identification, MB has also been reported in several other non-avian dinosaurs, including taxa outside the theropod lineage (Lee & Werning, 2008; Hübner, 2012), as well as pterosaurs (Prondvai & Stein, 2014; Prondvai, 2017). It has also been reported in two Mesozoic bird lineages recovered from the Jehol biota: in Confuciusornis (Chinsamy et al, 2013) and in two enantiornithines (an enantiornithine indet., O’Connor et al, 2018 and in Avimaia schweitzerae , Bailleul et al, 2019). Definitive evidence in support of this identification in Avimaia is provided through the preservation of an intra-abdominal egg, indicating this adaptation evolved outside the crown clade (Bailleul et al, 2019).…”

“…It has also been reported in two Mesozoic bird lineages recovered from the Jehol biota: in Confuciusornis (Chinsamy et al, 2013) and in two enantiornithines (an enantiornithine indet., O’Connor et al, 2018 and in Avimaia schweitzerae , Bailleul et al, 2019). Definitive evidence in support of this identification in Avimaia is provided through the preservation of an intra-abdominal egg, indicating this adaptation evolved outside the crown clade (Bailleul et al, 2019). However, because some pathologies can produce MB-like tissues in extant birds (Canoville, Schweitzer & Zanno, 2019), it has been noted that unambiguous identification of fossil tissues as reproductive MB requires more than just morphological similarity, particularly with increasing phylogenetic distance from the avian lineage, and/or when it appears in patterns different from those seen in extant birds (O’Connor et al, 2018).…”

“…Arguably, the most accurate way to assess sexual maturity in fossil dinosaurs and birds is to find skeletons in direct association with a clutch, or with unlaid eggs preserved internally (Sato et al, 2005; Erickson et al, 2007; Bailleul et al, 2019). However, medullary bone (MB), a female specific skeletal tissue formed during egg production, can also be used as a marker of reproductive activity (and thus reproductive maturity) if identified correctly.…”

“…Derived from the endosteum, MB can line the medullary cavities and cancellous spaces of the entire avian skeleton in some taxa (Canoville, Schweitzer & Zanno, 2019). In living birds, MB is estrogen dependent, forms extremely fast (although this might not have always been the case in stem taxa; see O’Connor et al, 2018; Bailleul et al, 2019), is high in calcium relative to other types of bone tissue, and is highly vascular, all which facilitate its function as an easily mobilized calcium reservoir (Bloom, Bloom & McLean, 1941; Taylor & Moore, 1953; Yamamoto et al, 2001).…”

A crocodylian-style cloaca in a non-avialan dinosaur

“…Despite the remarkable preservation of SMF R 4970, it was not possible to determine its sex. Although histological examination was not available, SMF R 4970 was not gravid, and therefore unlikely to have been producing medullary bone [23]. There is no evidence of a recognisable sexually dimorphic cloacal structure in SMF R 4970.…”