Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Abstract

Background: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stressesparticularly those produced through mastication of tough food itemsmay not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. Results: We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. Discussion: Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro-and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.

Skull shape of a widely distributed, endangered marsupial reveals little evidence of local adaptation between fragmented populations

“…However, there is an intriguing indication that at least some of the larger-scale evolutionary association between skull shape and size among marsupials may be visible at the within-species level. This is contrary to findings in other marsupials where feeding behaviors clearly influenced craniofacial morphology (Mitchell, Sherratt, Sansalone, et al, 2018;Weisbecker et al, 2019), and might represent one of several ways to shape morphological traits within the species.…”

“…This variation is consistent with well-known evolutionary adaptations to changes in mastication (Meloro, 2011;Mitchell, Sherratt, Sansalone, et al, 2018;Mitchell & Wroe, 2019;Weisbecker et al, 2019). The variation in muzzle length and zygomatic arch placement among some populations may be adaptations to a particular diet or feeding habit within each population.…”

“…It is common for mammals-particularly males-to display larger sagittal crests with age (Flores, Giannini, & Abdala, 2006), but this is a purely behavioral consequence of the pulling action of the temporalis muscle (Washburn, 1947). Similarly, bone remodeling during an individual's lifetime has been suggested for the zygomatic arch of mammals (Abdala & Giannini, 2000;Ravosa, 1991), and is also suspected in wombats and kangaroos Mitchell, Sherratt, Sansalone, et al, 2018;Weisbecker et al, 2019).…”

“…The shape of mammalian skulls contains information on animal function (Hanken & Hall, 1993), such as masticatory loading (Herring, Rafferty, Liu, & Marshall, 2001), acting as a proxy for dietary preferences in mammals (Maestri, Patterson, Fornel, Monteiro, & de Freitas, 2016; Marroig & Cheverud, 2005; Nogueira, Peracchi, & Monteiro, 2009), including marsupials (Mitchell, Sherratt, Ledogar, Sherratt, Ledogar, & Wroe, 2018; Wroe & Milne, 2007). This is particularly relevant in the context of marsupial mammals, whose skull might not be as adaptable as that of placental mammals due to a developmental constraint on skull shape variation (Goswami, Polly, Mock, & Sanchez‐Villagra, 2012; Porto, Shirai, de Oliveira, & Marroig, 2013; Sánchez‐Villagra, Goswami, Weisbecker, Mock, & Kuratani, 2008; Weisbecker, Goswami, Wroe, & Sanchez‐Villagra, 2008; Weisbecker et al., 2019). This is because marsupials are born at an extremely immature (altricial) state of development, but with a highly developed oral apparatus adapted to immediate and extensive feeding at the mother's teat.…”

Ontogenetic origins of cranial convergence between the extinct marsupial thylacine and placental gray wolf

“…The marsupial mode of reproduction requires accelerated morphogenesis and heterochronic gene expression in the forelimbs [40][41][42] and cranial bones 16,43 , which has been suggested to limit marsupial cranial disparity 38 and integration of the developing oral region 41 . However, the existence of marsupial "developmental constraint" has been challenged because marsupials have not always possessed limited diversity compared with placental mammals 44 , and do not appear to exhibit adaptive constraints on forelimb 45,46 or skull shape variation 47 . Nevertheless, despite these differences, the remarkable convergence of cranial shape between adult thylacines and wolves suggest the independent evolution of similar underlying developmental processes.…”