Functionally mediated cranial allometry evidenced in a genus of rock-wallabies

Abstract

In assessments of skeletal variation, allometry (disproportionate change of shape with size) is often corrected to examine size-independent variation for hypotheses relating to function. However, size-related trade-offs in functional demands may themselves be an underestimated driver of mammalian cranial diversity. Here, we use geometric morphometrics alongside dental measurements to assess craniodental allometry in the rock-wallaby genus Petrogale (all 17 species, 370 individuals). We identified functional aspects of evolutionary allometry that can be both extensions of, and correlated negatively with, static or ontogenetic allometric patterns. Regarding constraints, larger species tended to have relatively smaller braincases and more posterior orbits, the former of which might represent a constraint on jaw muscle anatomy. However, they also tended to have more anterior dentition and smaller posterior zygomatic arches, both of which support the hypothesis of relaxed bite force demands and accommodation of different selective pressures that favour facial elongation. By contrast, two dwarf species had stouter crania with divergent dental adaptations that together suggest increased relative bite force capacity. This likely allows them to feed on forage that is mechanically similar to that consumed by larger relatives. Our results highlight a need for nuanced considerations of allometric patterns in future research of mammalian cranial diversity.

Beyond CREA: Evolutionary patterns of non‐allometric shape variation and divergence in a highly allometric clade of murine rodents

“…The high integration between the rostrum and the cranial vault in the full dataset is predicted by CREA, and is notable because it supports the hypothesis of Mitchell, Potter, et al. ( 2024 ); Mitchell, Sherratt, and Weisbecker ( 2024 ) that CREA is a mosaic arising from different mechanisms; in rodents, this would be bite force allometry affecting the rostral area combined with hypo‐allometry of the brain affecting the cranial vault. Consistent with CREA patterns being driven mostly by allometry, the integration between the vault and the rostrum also drops most dramatically after the removal of size.…”

“…In addition to the strong CREA pattern, and consistent with Mitchell, Potter, et al. 's ( 2024 ); Mitchell, Sherratt, and Weisbecker's ( 2024 ) predictions, Marcy et al. ( 2020 ) noted that species whose shape departed most from the common evolutionary allometric pattern tended to be ecological specialists with distinct diets and locomotor modes.…”

“…Many studies of mammalian cranial shape evolution are consistent with the concept of CREA as a result of biomechanics (e.g. Cardini et al., 2015 ; Figueirido et al., 2013 , 2014 ; Tamagnini et al., 2017 , 2023 ), and the effect was recently demonstrated in a genus of marsupial rock‐wallabies (Mitchell, Potter, et al., 2024 ). However, the view in Mitchell, Sherratt, and Weisbecker ( 2024 ) suggests that CREA reflects one part of biomechanical evolution as far as it pertains to allometry, but that changes in dietary regime will result in shape changes not captured by CREA.…”

“…Allometry in mammalian crania, and the associated shape variation as predicted by CREA, has often been attributed to the integration of size with masticatory biomechanics (Marroig & Cheverud, 2005 ; Mitchell et al., 2018 ; Mitchell, Potter, et al., 2024 ; Singleton, 2005 ; Weisbecker et al., 2019 ). This is probably particularly true for rodents, where high levels of allometry likely reflect constraints imposed by their highly derived gnawing function (Cox et al., 2012 ; Druzinsky, 2015 ; Ginot et al., 2018 ; Lessa & Patton, 1989 ; Marcy et al., 2016 , 2020 ).…”

“…Possibly for this reason, cranial morphology across mammals displays some common patterns of evolutionary variation. The most widely discussed of these is the tendency of larger mammals to have more elongate facial skeletons and smaller braincases relative to smaller species, particularly in closely related species (Cardini et al., 2015 ; Cardini & Polly, 2013 ; Mitchell, Potter, et al., 2024 ; Tamagnini et al., 2017 ). This pattern, termed craniofacial evolutionary allometry (CREA), exists in at least 11 vertebrate orders, especially those of mammals (Bright et al., 2016 ; Cardini, 2019 ), but the origins of this pattern have been unclear (e.g.…”