Eggshell Porosity Provides Insight on Evolution of Nesting in Dinosaurs

<div><p>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 <i>Lourinhanosaurus</i> 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).</p></div

List of equations used for this study, modified from Tanaka and Zelenitsky [18].

<p>List of equations used for this study, modified from Tanaka and Zelenitsky [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0142829#pone.0142829.ref018" target="_blank">18</a>].</p

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

<p>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.</p

List of variables used for this study, modified from Tanaka and Zelenitsky [18].

<p>List of variables used for this study, modified from Tanaka and Zelenitsky [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0142829#pone.0142829.ref018" target="_blank">18</a>].</p

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

<p>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.</p

Results of conventional OLS regression models for living archosaur species.

<p>Abbreviations: CI, 95% confidence interval; n, sample size; r², coefficient of determination.</p><p>Results of conventional OLS regression models for living archosaur species.</p

Cross-classification/ confusion matrix from LDA and pFDA.

<p>The true classifications are along the top and the predicted classifications are on the left-hand side.</p><p>Cross-classification/ confusion matrix from LDA and pFDA.</p

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

<p>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 <i>Lourinhanosaurus</i>, which change to open nesters when lambda values approach one. The yellow line indicates the optimal lambda value (0.56).</p

List of extinct archosaur taxa/ootaxa with estimated egg mass (M) and eggshell porosity (A_p∙Ls-1) used in this study.

<p>Asterisk (*) indicates that eggshell thickness was taken from Zhao [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0142829#pone.0142829.ref043" target="_blank">43</a>] because Mou [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0142829#pone.0142829.ref041" target="_blank">41</a>] provided only the thickness of the continuous layer as pore length.</p><p>List of extinct archosaur taxa/ootaxa with estimated egg mass (M) and eggshell porosity (A_p∙Ls-1) used in this study.</p

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

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