A Simple Skeletal Measurement Effectively Predicts Climbing Behaviour in a Diverse Clade of Small Mammals
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applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Biological Journal of the Linnean Society, 2019, 128, 323–336. With 5 figures. A simple skeletal measurement effectively predicts climbing behaviour in a diverse clade of small mammals JONATHAN A. NATIONS1,2,*, , LAWRENCE R. HEANEY3, TERRENCE C. DEMOS3, Downloaded from https://academic.oup.com/biolinnean/article-abstract/128/2/323/5533433 by guest on 17 September 2019 ANANG S. ACHMADI4, KEVIN C. ROWE5 and JACOB A. ESSELSTYN1,2 1Museum of Natural Science, 119 Foster Hall, Louisiana State University, Baton Rouge, LA 70803, USA 2Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA 3Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA 4Museum Zoologicum Bogoriense, Research Centre for Biology, Cibinong, Jawa Barat 16911, Indonesia 5Sciences Department, Museum Victoria, Melbourne, VIC 3001, Australia Received 2 April 2019; revised 16 May 2019; accepted for publication 16 May 2019 Arboreal locomotion allows access to above-ground resources and might have fostered the diversification of mammals. Nevertheless, simple morphological measurements that consistently correlate with arboreality remain indefinable. As such, the climbing habits of many species of mammals, living and extinct, remain speculative. We collected quantitative data on the climbing tendencies of 20 species of murine rodents, an ecologically and morphologically diverse clade. We leveraged Bayesian phylogenetic mixed models (BPMMs), incorporating intraspecific variation and phylogenetic uncertainty, to determine which, if any, traits (17 skeletal indices) predict climbing frequency. We used ordinal BPMMs to test the ability of the indices to place 48 murine species that lack quantitative climbing data into three qualitative locomotor categories (terrestrial, general and arboreal). Only two indices (both measures of relative digit length) accurately predict locomotor styles, with manus digit length showing the best fit. Manus digit length has low phylogenetic signal, is largely explained by locomotor ecology and might effectively predict locomotion across a multitude of small mammals, including extinct species. Surprisingly, relative tail length, a common proxy for locomotion, was a poor predictor of climbing. In general, detailed, quantitative natural history data, such as those presented here, are needed to enhance our understanding of the evolutionary and ecological success of clades. ADDITIONAL KEYWORDS: arboreal – comparative method – ecomorphology – manus index – Murinae – Philippines – phylogenetic mixed models. INTRODUCTION behaviour does not fossilize, our understanding of the role of climbing in the history of placental mammal Climbing is a key behaviour that facilitates access radiation is derived from indirect inferences from to above-ground resources and hence, ecological skeletal morphology (Ji et al., 2002; Luo et al., 2003; opportunity. As such, the tendency to climb might Kirk et al., 2008; Samuels & Van Valkenburgh, 2008; have altered patterns of competition and processes Chen &Wilson, 2015; Meng et al., 2017). of diversification in the evolutionary history of many Similar to the situation for extinct mammals, vertebrate clades, including mammals (Jenkins, the locomotor behaviour of many living species is 1974a; Scheffers et al., 2013; Bars-Closel et al., unknown. Most small mammals (< 5 kg) are nocturnal 2017; de Alencar et al., 2017). Scansoriality, i.e. the and secretive, making observations difficult, and it is propensity to climb, might be the ancestral locomotor mode of placental mammals (O’Leary et al., 2013), and not uncommon for researchers to discover climbing recent paleontological work suggests that climbing behaviour in common, widespread species long thought facilitated placental mammal diversification (Ji et al., of as exclusively terrestrial (Ingles, 1960; Nations & 2002; Luo et al., 2011). However, because locomotory Olson, 2015; Costa et al., 2017). Exploiting the arboreal niche requires the ability to navigate the trunks and branches of trees while *Corresponding author. E-mail: [email protected] simultaneously performing basic activities, such as © 2019 The Linnean Society of London, Biological Journal of the Linnean Society, 2019, 128, 323–336 323 324 J. A. NATIONS ET AL. feeding. Arboreal substrates range from horizontal to to have high scores for this axis, it is challenging to vertical and vary dramatically in diameter and texture. disentangle which, if any, of these three traits can be In vertebrates, there are a variety of solutions to the used to infer climbing affinity. physical challenges of arboreality, such as the adhesive Unlike other ecomorphological model systems, such as toepads found in some squamates. In general, climbing Anolis lizards (Losos, 2009), small mammal body mass may mammals rely on increased grip and claw purchase, span three orders of magnitude. This might be important, improved depth perception and the use of the tail because smaller-bodied arboreal and terrestrial species for balance, stability or grasping (Cartmill, 1985; have been shown to be more similar morphologically than Tulli et al., 2015). Given that the differences between larger-bodied species, probably owing to the mechanics of Downloaded from https://academic.oup.com/biolinnean/article-abstract/128/2/323/5533433 by guest on 17 September 2019 terrestrial locomotion and climbing are substantial, it locomotion (Kirk et al., 2008). Additionally, non-primate is thought that both behavioural and morphological models span the mammalian phylogeny, from marsupials adaptations occur in concert with transitions between to murids, or ~175 Myr of evolutionary time (Meredith these ecological states. A signal of morphological et al., 2011), and it remains unclear whether shared traits adaptations to arboreal locomotion might be found are attributable to morphological convergence or are in the postcranial skeletons of climbing mammals simply historical artefact. Recent work has successfully (Jenkins, 1974a; Cartmill, 1985). used three-dimensional morphometrics and muscular Identifying which, if any, skeletal characters structure to identify differences indicative of climbing accurately predict climbing behaviour would facilitate in non-primate mammals (Fabre et al., 2013a; Taverne locomotor inferences for both extinct species and et al., 2018), but these methods lack the simplicity needed living species that lack observational data. Connecting to infer locomotion for the numerous extant and extinct morphology with locomotor behaviours requires a species with no behavioural data. Ideally, inferences of study system with species spanning a range of body climbing behaviour should be based on simple characters sizes, quantitative observations of the propensity to that commonly fossilize and are either indicative of climb, and a strong understanding of phylogenetic climbing regardless of size or are known to be relevant for relationships to account for the non-independence organisms of a given size. of traits (Harvey & Pagel, 1991). Although primates The rodent subfamily Murinae (Rodentia: Muridae) represent only one of numerous independent origins of contains 704 recognized species, 11% of extant scansoriality in mammals, they have been the subject of mammals, that encompass a wide range of locomotor most climbing studies to date (Jenkins, 1974a, b; Gebo, ecomorphologies, from semi-aquatic and semi-fossorial 1996, 2004; Bloch & Boyer, 2002; Kirk et al., 2008). to arboreal (Musser & Carleton, 2005; Pagés et al., Most primate species have such extreme adaptations 2015; Rowe et al., 2016; Burgin et al., 2018). Climbing to climbing that they might be poor models for how murines vary in mass and behaviour, from the large climbing generally evolves (Jenkins, 1974b); therefore, canopy-dwelling cloud rats (Phloeomys; ≤ 2.7kg), to the transition from the ground to the trees has been the tiny bamboo-nesting Ranee mice (Haeromys; investigated in various small, non-primate species, < 10 g). Terrestrial murines span a similar breadth which vary in size from ~15 g to 6 kg (Argot, 2002; of body sizes. This size range provides an opportunity Urbani & Youlatos, 2013). to quantify traits unique to, and shared between, Skeletal traits traditionally associated with functional groups and to determine whether and how climbing in non-primate models include equal limb those traits vary with respect to body size. proportions, long digits, long tail and mobile ankle The Philippines is home to ~80 currently recognized, joints (Argot, 2002; Ji et al., 2002; Sargis, 2002a, b; mostly endemic murine species (Heaney et al., 2016), Kirk et al., 2008; Samuels & Van Valkenburgh, 2008; resulting from five radiations within four murine Woodman & Stabile, 2015). However, when analysed ‘divisions’ (Jansa et al., 2006; Rowe et al., 2016). Three in multivariate morphospace, as is common practice of these clades (cloud rats, earthworm mice and ‘true’ in other vertebrate systems (e.g. Mahler et al., 2013; rats) contain both terrestrial and scansorial forms, Ingram & Kai, 2014), small climbing and terrestrial allowing for direct comparison between closely related forms often overlap (Kirk et al., 2008; Samuels & Van but behaviourally divergent species. Uniquely, these Valkenburgh, 2008; Verde Arregoitia et al., 2017). This species are well represented by voucher specimens pattern is potentially explained by the less extreme with complete postcranial skeletons and detailed adaptations