Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill

Abstract

The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as Triceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.

Three-dimensional geometric morphometric analysis of the skull of Protoceratops andrewsi supports a socio-sexual signalling role for the ceratopsian frill

“…Although all modules showed some degree of change, the parietal-squamosal frill consistently displayed the highest rates of size and shape change through ontogeny, as well as the highest morphological variance independent of size, expanding significantly during ontogeny to form a large, conspicuous structure (figure 3a,b). The accelerated growth rate of the frill when compared with the remainder of the skull adds further support to the hypothesis that this structure evolved as a socio-sexual signal, and probably evolved via heterochrony [29]. There are two important differences between our allometry analyses and those in previous studies [13,19,33].…”

“…We found strong support for a five-module model of the cranium of P. andrewsi. Although the treatment of the frill as a distinct module [ 29 , 34 ] is supported by our analysis, it is clear from these results that cranial modularity of P. andrewsi is more complex than a simple division of frill and remainder of the skull. Modularity suggests that regions of the skull independently vary in their rate of growth, ontogenetic shape change and morphological variance.…”

“…Positive allometry, an increased relative change in size and shape, is typical of many socio-sexual traits during growth (ontogenetic allometry), and among individuals of the same species and developmental stage (static allometry) [ 19 , 27 ]. Ontogenetic allometry occurs because as animals become sexually mature the importance of socio-sexual traits changes, meaning that the optimal form will vary accordingly with the animal's growth [ 27 , 28 ], and probably evolves through heterochrony [ 29 ]. Positive static allometry is expected to occur in a socio-sexual trait when the relative size of the trait in question is an ‘honest’ signal of condition or resource-holding potential, resulting in small differences in body size being reflected in proportionally larger differences in trait size [ 19 ].…”

“…The ceratopsian dinosaur Protoceratops andrewsi possessed a large frill projecting caudally from the skull, formed from enlargement of the parietal and squamosal bones (electronic supplementary material, figure S1). This frill has previously been suggested as a potential sexual or socio-sexual signal, and positive allometry [ 13 ], modularity [ 29 ] and sexual dimorphism [ 33 , 34 ] have all been assessed using different measurements. Protoceratops andrewsi , being one of the few dinosaur examples with sufficient well-preserved specimens available to allow an in-depth analysis of morphology and variation, is an ideal candidate for examining intraspecific variation in non-avian dinosaurs, but a clear picture of the function of the frill has yet to emerge.…”

SPASOS 1.1: a program for the inference of ancestral shape ontogenies

“…Studies that include the phylogenetic dimension in GM analyses have been oriented to evaluate a variety of questions including shape/function relationship (Cooke and Terhune, 2015;Borgard et al, 2020), shape covariation (Machado et al, 2018), rates of evolutionary change (Houle et al, 2017;Santos et al, 2019), morphological evolution (Stayton, 2004;Duport Bru et al, 2019;Segura et al, 2021), morphological disparity (Stange et al, 2018;Schaeffer et al, 2019), and phylogenetic inference (Ascarrunz et al, 2019). In particular, the role of changes in developmental timing in generating the shape diversity has been the subject of several recent studies in both extant (Esquerré et al, 2017;Morris et al, 2019;Sherratt et al, 2019) and fossil species (Maiorino et al, 2013;Foth et al, 2016;Prieto-Márquez et al, 2020). Most phylogenetic approaches to analyze GM data involve a step where ancestral shapes and changes in shape along the tree are established.…”