Scaling patterns of body plans differ among squirrel ecotypes

Abstract

Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size (i.e., body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels.

Size and locomotor ecology have differing effects on the external and internal morphologies of squirrel (Rodentia: Sciuridae) limb bones

“…4; Fig. 6), consistent with previous findings (Peterka 1936; Bryant 1945; Thorington and Heaney 1981; Grossnickle et al 2020; Linden et al 2023).…”

“…Allometric patterns in bone structure variables are further nuanced by ecological specialization. In ground squirrels, positive allometry of limb bone structures is consistent with positive allometry of more robust body shapes (Linden et al 2023), which together may serve as adaptations for the digging and clearing stages of scratch digging during burrow construction. The digging stage consists of the claws of the forelimbs striking the ground while the hind limbs supports the body (Gasc et al 1985; Hildebrand 1995), and a plethora of skeletal and muscular adaptations in the forelimb are associated with this first stage (Lessa and Stein 1992; Hildebrand 1995; Lagaria and Youlatos 2006; Vassallo 2006; Steiner-Souza et al 2010).…”

“…Following Linden et al (2023), we categorized species into four ecotypes-chipmunk (n = 14), gliding (n = 8), ground (n = 25), or tree (n = 29)-based on either locomotion, evolutionary grouping, or reproductive behavior (Fig. 1).…”

“…While the influence of body size on external limb bone morphology has been researched extensively, relatively fewer studies have examined bone structural characteristics such as bone compactness, second moment of area, or cross-sectional shape, even though these traits affect the mechanics and locomotor ecologies of species (Amson et al 2022). Additionally, the interaction between allometry and ecological effects on limb bone morphology has received little attention, despite implications about how different locomotory modes may affect overall limb bone evolution (Hayssen 2008; Wölfer et al 2019; Linden et al 2023). The internal structure of bone is highly plastic (Amson et al 2018) due to the ability of bone tissue to remodel in response to its mechanical environment (i.e., Wolff’s Law) (Dawson 1980; Ruff et al 2006; Meier et al 2013; Kivell 2016).…”

“…Squirrel species can be categorized into four ecotypes with distinct locomotor ecologies and behaviors: ground squirrels that dig, tree squirrels that climb, gliding squirrels that glide between trees, and more versatile chipmunks that both dig and climb. Previous work has examined relationships between limb lengths and ecotypes, finding, for example, that gliding squirrels exhibit relatively longer forelimbs than all other ecotypes (Peterka 1936; Bryant 1945; Thorington and Heaney 1981; Grossnickle et al 2020; Linden et al 2023) and ground squirrels exhibit relatively shorter forelimbs with increasing body elongation (Linden et al 2023). Furthermore, across Sciuromorpha (squirrel-like rodents), cross-sectional characteristics (i.e., cross-sectional area and second moment of area) of the femur scale with positive allometry with respect to body mass (Scheidt et al 2019).…”