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. 2019 Jun 12;286(1904):20190409.
doi: 10.1098/rspb.2019.0409. Epub 2019 Jun 12.

Prenatal development in pterosaurs and its implications for their postnatal locomotory ability

Affiliations

Prenatal development in pterosaurs and its implications for their postnatal locomotory ability

David Michael Unwin et al. Proc Biol Sci. .

Abstract

Recent fossil finds in China and Argentina have provided startling new insights into the reproductive biology and embryology of pterosaurs, Mesozoic flying reptiles. Nineteen embryos distributed among four species representing three distinct clades have been described and all are assumed to be at, or near, term. We show here how the application of four contrasting quantitative approaches allows a more precise identification of the developmental status of embryos revealing, for the first time to our knowledge, the presence of middle and late developmental stages as well as individuals that were at term. We also identify a predicted relationship between egg size and shape and the developmental stage of embryos contained within. Small elongate eggs contain embryos at an earlier stage of development than larger rounder eggs which contain more fully developed embryos. Changes in egg shape and size probably reflect the uptake of water, consistent with a pliable shell reported for several pterosaurs. Early ossification of the vertebral column, limb girdles and principal limb bones involved some heterochronic shifts in appearance times, most notably of manus digit IV, and facilitated full development of the flight apparatus prior to hatching. This is consistent with a super-precocial flight ability and, while not excluding the possibility of parental care in pterosaurs, suggests that it was not an absolute requirement.

Keywords: egg; embryology; heterochrony; locomotion; mesozoic; pterosaur.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1.
Figure 1.
Predicted EM plotted against egg elongation for eggs of H. tianshanensis without (open circles) and with embryos (filled circles: embryos 5, 11 and 12 of Wang et al. [8]), a second pterosaur from the Lower Cretaceous of Hami (triangle), and two ornithocheirid pterosaurs (grey diamonds) from the Yixian Formation [1,2]. Outlines of Hamipterus eggs illustrate relationship between shape and mass. See the electronic supplementary material, tables S1 and S2 for data.
Figure 2.
Figure 2.
Humerus length as a proportion of forelimb length plotted against forelimb length (mm) for a sample of pterosaur embryos, hatchlings and immature individuals with humeri ranging from 12 to 20 mm in length. Solid symbol, embryo; open symbol, hatchling or immature individual. (a) SMNS 81928 (cast); (b) IVPP V13758; (c) IVPP V18943, embryo 13; (d) BSP 1964 XXIII 100; (e) MIC V246; (f) IVPP V18942. Humeri drawn to scale and shown in the lateral view. Scale bar, 5 mm. (a) Redrawn from [20]; (b) modified from [2]; (c) and (f) redrawn from [8]; (d) redrawn from [21]; (e) modified from [22]. (See the electronic supplementary material, table S4 for complete dataset). Trend lines are least square regressions generated by Excel (see the electronic supplementary material, table S4). (Online version in colour.)
Figure 3.
Figure 3.
Ossification of the skeleton in pterosaur embryos. (a) Comparison of mid-term embryos (left) and near-term embryos (right). Scale bar, 5 mm. Redrawn from [2,8,22]. (b) Degree of ossification of principal skeletal elements in four pterosaur embryos, calibrated against a hatchling and two immature individuals. (c) Comparison of developmental stages in A. mississippiensis with four pterosaur embryos. Symbols: dark grey fill, skeletal structure well ossified/teeth erupted or, in A. mississippiensis, any degree of ossification; light grey fill, skeletal structure poorly ossified: no fill, absence of element inferred to be owing to lack of ossification; X, ossified element inferred to have originally been present, but now obscured by overlying elements, buried or lost owing to postmortem damage; ?, uncertain identification of element. Em, embryo; Ha, hatchling; Im, immature; OS, ontogenetic status; Am, Al. mississippiensis, Ht, H. tianshanensis; Or, Ornithocheiridae gen et sp. indet., Pg, P. guinazui; Pk, Pterodactylus kochi; Rm, R. muensteri; Ca, carpals; Cd, caudal vertebrae; Co, coracoid; Cr, cranium; Cv cervical vertebrae; De, dentition; Do, dorsal vertebrae; Fe, femur; Ga, gastralia; Hu, humerus; Ma, mandibles; MI–III, manual digits I–III; MIV, manual digit IV; McI–III, metacarpals I–III; McIV, metacarpal IV; Mt, metatarsals; Pe, pelvis, Pd, pedal digits; Ri, ribs, Ro, rostrum; R/U, radius/ulna; Sa, sacral vertebrae; Sc, scapula, Sk, skull; Ta, tarsals; T/F tibia/fibula; W1, 2, 3, 4, wing-finger phalanges 1, 2, 3, 4. See the electronic supplementary material, table S1 for sources of data.
Figure 4.
Figure 4.
Fossil record of prenatal and early postnatal development in pterosaurs. Darwinopterus modularis (a) ZMNH M8802. Hamipterus tianshanensis (b1–3) outlines of egg shape illustrating changes in size and shape; (c) IVPP V18942 embryo 5; (d) IVPP V18941 embryo 11; (e) IVPP V18942 embryo 12; (f) IVPP V18943 humerus of embryo 13; (j) IVPP V18942 hatched? egg; (k) IVPP V18942 humerus. Ornithocheiridae genus et sp. indet. (g) IVPP V13758 embryo. Pterodaustro guinazui (h) MIC V246, embryo; (l) MIC V241 hatchling. Pterodactylus kochi (m) BSP 1967 I 276. Not to scale. (c–f,j,k) redrawn from [8], (g) redrawn from [2], (h) redrawn from [22], (l) redrawn from [28]; (m) redrawn from [21]. (Online version in colour.)

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