Eggshell Porosity Provides Insight on Evolution of Nesting in Dinosaurs

Abstract

Knowledge about the types of nests built by dinosaurs can provide insight into the evolution of nesting and reproductive behaviors among archosaurs. However, the low preservation potential of their nesting materials and nesting structures means that most information can only be gleaned indirectly through comparison with extant archosaurs. Two general nest types are recognized among living archosaurs: 1) covered nests, in which eggs are incubated while fully covered by nesting material (as in crocodylians and megapodes), and 2) open nests, in which eggs are exposed in the nest and brooded (as in most birds). Previously, dinosaur nest types had been inferred by estimating the water vapor conductance (i.e., diffusive capacity) of their eggs, based on the premise that high conductance corresponds to covered nests and low conductance to open nests. However, a lack of statistical rigor and inconsistencies in this method render its application problematic and its validity questionable. As an alternative we propose a statistically rigorous approach to infer nest type based on large datasets of eggshell porosity and egg mass compiled for over 120 extant archosaur species and 29 archosaur extinct taxa/ootaxa. The presence of a strong correlation between eggshell porosity and nest type among extant archosaurs indicates that eggshell porosity can be used as a proxy for nest type, and thus discriminant analyses can help predict nest type in extinct taxa. Our results suggest that: 1) covered nests are likely the primitive condition for dinosaurs (and probably archosaurs), and 2) open nests first evolved among non-avian theropods more derived than Lourinhanosaurus and were likely widespread in non-avian maniraptorans, well before the appearance of birds. Although taphonomic evidence suggests that basal open nesters (i.e., oviraptorosaurs and troodontids) were potentially the first dinosaurs to brood their clutches, they still partially buried their eggs in sediment. Open nests with fully exposed eggs only became widespread among Euornithes. A potential co-evolution of open nests and brooding behavior among maniraptorans may have freed theropods from the ground-based restrictions inherent to covered nests and allowed the exploitation of alternate nesting locations. These changes in nesting styles and behaviors thus may have played a role in the evolutionary success of maniraptorans (including birds).

Fig 1. Porosity of archosaur eggshell.

Schematic diagram of archosaur eggshell with high porosity (A) and low porosity (B), modified from [18]; tangential thin sections of living covered nester Caiman latirostris (C), living open nester Pavo cristatus (D), and non-avian maniraptoran Troodon formosus (E). Abbreviations; A, individual pore area; D, pore density; L_s, pore length. Arrows indicate pore canals.

Fig 2. Bivariate plot of eggshell porosity and egg mass between living covered and open nesters.

Eggshell porosity relative to egg mass is highly correlated to nest types (p < 0.01), as reflected by the different regression models between closed and open nesters.

Fig 3. Bivariate plot of eggshell porosity and egg mass in both living and extinct archosaur taxa/ootaxa.

Titanosaurs and Lourinhanosaurus show high eggshell porosity, comparable to living species with covered nests. In contrast, oviraptorosaurs, Troodon, and moas show lower eggshell porosity, similar to species with open nests.

Fig 4. Misclassification rate of pFDA for living species through changing Pagel's lambda values.

Dash line shows the optimal lambda value of 0.56. Note that the overall misclassification rate increases with increasing lambda values from 0 to 1.

Fig 5. Comparison of the discriminant function between covered and open nesters in living and fossil archosaurs.

Horizontal bars inside boxes represent medians, lower and upper ends of boxes are the 25% and 75% quartiles, respectively, and whiskers represent the smallest and largest cases. Outliers are represented by dots and extremes by diamonds. Note that covered nesters show relatively lower values than open nesters.

Fig 6. Inferred nest type for six extinct archosaurs as a function of Pagel's lambda values.

Inferred nest type is generally consistent across all lambda values, except for oviraptorosaurs where inferred nest type changes when the lambda value varies between 0.08 and 0.52, and for titanosaurs and Lourinhanosaurus, which change to open nesters when lambda values approach one. The yellow line indicates the optimal lambda value (0.56).

Fig 7. Evolution of nest types among archosaurs.

(A) Phylogeny of archosaurs with inferred nest types based on eggshell porosity and taphonomic evidence. Covered nests are the primitive condition for dinosaurs; open nests and brooding behavior were present among non-avian maniraptoran theropods but may have first appeared earlier. Although the eggs of early open nesters were still partially covered by substrate, open nests with fully exposed eggs likely arose among Euornithes. (B) Phylogeny of Neornithes with inferred nest types based on eggshell porosity (Emeidae) and literature (other birds). Open nests with fully exposed eggs are the primitive condition for modern birds, although secondary reversal to partial egg burial occurred independently in several clades. Information for bird orders which include species that partially bury the eggs (Charadriiformes) or occasionally cover the eggs in open nests (Accipitriformes, Anseriformes, Charadriiformes, Gruiformes, Passeriformes, Podicipediformes, Struthioniformes, Tinamiformes) was taken from [–103]. Cladograms are based on [,,–106].