Comparative Morphology of the Dormouse Skull
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bioRxiv preprint doi: https://doi.org/10.1101/2021.04.23.441073; this version posted April 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Title: Comparative morphology of the dormouse skull Author: Jesse J. Hennekam1,2 Affiliations: 1Naturalis Biodiversity Center, Leiden, The Netherlands 2Hull York Medical School, University of York, United Kingdom Corresponding author: Jesse J. Hennekam Address: 1Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands 2PalaeoHub, University of York, Wentworth Way, York, YO10 5DD, UK Email: [email protected] 1 Comparative morphology of the dormouse skull - Preprint bioRxiv preprint doi: https://doi.org/10.1101/2021.04.23.441073; this version posted April 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Abstract Dormice exhibit both inter- and intrageneric variation in cranial and mandibular morphology. Using geometric morphometrics, the form of eight out of nine extant dormouse genera was analysed, to provide a better understanding of the overall morphological variation present within Gliridae. Three genera representing the subfamilies, were studied in more detail. Species-, genus- and family-specific morphological trends are linked with certain habitats and feeding strategies. Smaller dormice show adaptations to a more arboreal lifestyle such as a relatively enlarged braincase and an inferiorly reoriented foramen magnum. Larger dormice show cranial modifications, including clear flattening of the skull and a more posteriorly positioned foramen magnum, hinting towards a more rupicolous lifestyle. Furthermore, specimens inhabiting arid areas appear to have more inflated auditory bullae, whereas other variable features, such as the length of the incisive foramen, were not associated with either size changes nor climatic variables. Lastly, more robust and horizontally orientated zygomatic arches as well as increased robusticity of the molar row appear to be linked with herbivory in dormice, whereas thinner arches and small concave molars are seen in more insectivorous species. This study results in a better understanding of ecological drivers underpinning the morphological divergence present within Gliridae. Keywords Dormice; Gliridae; Geometric Morphometrics; Allometry; Skull Morphology; Functional Morphology 2 Comparative morphology of the dormouse skull - Preprint bioRxiv preprint doi: https://doi.org/10.1101/2021.04.23.441073; this version posted April 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Introduction Gliridae is considered one of the oldest extant rodent families (Fabre et al., 2012) and consists of nine dormouse genera split over three subfamilies; Glirinae (Glirulis, Glis), Leithiinae (Chaetocauda, Dryomys, Eliomys, Muscardinus, Myomimus and Selevinia), and the monogeneric Graphiurinae (Graphiurus) (Holden-Musser et al., 2016). Dispersed widely throughout Africa and Eurasia, the family occupies various ecological habitats, including tropical forests in Africa and deserts in central Asia. Dormouse species vary significantly in both cranial and mandibular morphology, with some of these morphological variations thought to be related to adaptations to specific habitats and diet (Wahlert et al., 1993; Hennekam et al., 2020a). The fossil record shows the radiation of Gliridae to start during the Early Eocene (Vianey-Liaud, 1994), with the opening of the North Atlantic, and to peak around the late Early Miocene (Daams & de Bruijn, 1995). During this time, dormice were especially abundant and diverse within the Mediterranean area (Hartenberger, 1994), occupying a variety of different ecological niches and exhibiting a great diversity in diet, as evidenced by, for example, the evolution of a hypsodont species (Freudenthal & Martin-Suarez, 2013). The extant dormouse distribution is only a remnant of the success of this family in the past; nonetheless, the various ecological niches occupied by these species today suggest that adaptability to different environments is still retained within the family. Morphological diversification within animals has been thoroughly investigated in an evolutionary context (e.g. Cardini, 2003; Cardini et al., 2004, 2005; Monteiro et al., 2005; Caumul & Polly, 2005; Michaux et al., 2008). However, these studies often only describe morphological variation at a species or genus level (e.g. Cardini et al., 2004; Ferreira-Cardoso et al., 2020). Morphometrics at a family level sometimes requires the analysis of large numbers of specimens to represent the full extent of this taxonomic rank. Despite some families containing only a small number of species, e.g. Castoridae (2 species), Pedetidae (2) and Aplodontiidae (1), many rodent families are quite species-rich (Burgin et al., 2018). Thus, often a subset of these large families is analysed in order to make the study more comprehensible, as has been done, for example, in the case of Sciuridae (Michaux et al., 2008; Lu et al., 2014). A large number of specimens can often necessitate the use of 2D morphometrics, in which the lack of the third dimension can have significant impact on the strength of the conclusions that can be drawn (Roth, 1993; Álvarez & Perez, 2013; Cardini, 2014; Bakkes, 2017). In particular, more subtle (intra- specific) morphological variation is affected by the inaccuracies seen in 2D datasets (Cardini & Chiappelli, 2020). Fortunately, the increased affordability of 3D scanning of osteological material has a clear positive impact on morphometric studies of large 3D datasets (e.g. Marcy et al., 2018, Ferreira- Cardoso et al., 2020). Gliridae is a relatively small family within Rodentia with only 29 species in 9 genera (Holden-Musser et al., 2016), making it a tractable group for analyzing morphological variations with respect to size, phylogeny and ecology at this taxonomic level. Previous studies have analysed the cranium within extant dormice (Wahlert et al., 1993; Daams & de Bruijn, 1995; Koenigswald, 1995; Potapova, 2001; Hautier et al., 2008; Hennekam et al., 2020a) and found large variation in, for example, the zygomasseteric construction, morphology of the auditory bullae, and dental characteristics. In particular, the subfamily Graphiurinae appears to differ significantly from other dormice, resulting in much debate on its phylogenetic position within the family (Winge, 1941; Simpson, 1945; Vianey-Liaud & Jaeger, 1996). Molecular phylogenetic studies have not been conclusive for Gliridae, resulting in the positioning of some genera and species remaining unresolved (Bentz & Montgelard, 1999; Montgelard et al., 2003; Nunome et al., 2007). 3 Comparative morphology of the dormouse skull - Preprint bioRxiv preprint doi: https://doi.org/10.1101/2021.04.23.441073; this version posted April 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Figure 1 Lateral view of crania and mandibles representing all the species used in this study. Colours are associated to datapoints in subsequent figures referring to the genus. The same scale is used for all specimen. 4 Comparative morphology of the dormouse skull - Preprint bioRxiv preprint doi: https://doi.org/10.1101/2021.04.23.441073; this version posted April 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Aims The considerable morphological variation, but relatively low number of species within Gliridae mas it an excellent candidate for a case study investigating adaptive morphological features within a group at species, genus and (sub)family level. Using geometric morphometrics, this study aims to characterise the morphological variation present in the crania and mandibles of dormice and to assess the relationship between morphology and ecology. All but one of the genera comprising Gliridae are represented in the study, resulting in a nearly complete morphological overview of this family. The following three hypotheses will be addressed: Intrageneric morphological variation within dormice is less pronounced than intergeneric variation. Clear morphological variation is present both between (Wahlert et al., 1993; Hennekam et al., 2020a), and within dormouse genera (Storch, 1978 and Figure 1). In order to understand the morphological traits within this family, the extent of this inter- and intrageneric morphological variation will be analysed. Given that certain genera are highly specialized to specific habitats (e.g. the desert dormouse Selevinia), traits that vary between genera are expected. However, intrageneric morphological variation is also expected for specimens occupying various ecoregions. By evaluating the morphological variation