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Sectional Geometry in a Simulated Fine Branch Niche JOURNAL OF MORPHOLOGY 276:759–765 (2015) Mouse Hallucal Metatarsal Cross-Sectional Geometry in a Simulated Fine Branch Niche Craig D. Byron,1* Anthony Herrel,2,3 Elin Pauwels,4 Amelie De Muynck,4 and Biren A. Patel5,6 1Department of Biology, Mercer University, Macon, Georgia 2Departement d’Ecologie et de Gestion de la Biodiversite, CNRS/MNHN, Paris, France 3Department of Vertebrate Evolutionary Morphology, Ghent University, Gent, Belgium 4Department of Physics and Astronomy, Ghent University, UGCT, Ghent, Belgium 5Department of Cell and Neurobiology, Keck School of Medicine, University of Southern California, Los Angeles, California 6Human and Evolutionary Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California ABSTRACT Mice raised in experimental habitats con- arboreal substrates (Le Gros Clark, 1959; Cart- taining an artificial network of narrow “arboreal” sup- mill, 1972; Szalay and Drawhorn, 1980; Sussman, ports frequently use hallucal grasps during locomotion. 1991; Schmitt and Lemelin, 2002; Bloch et al., Therefore, mice in these experiments can be used to 2007; Sargis et al., 2007). There are also examples model a rudimentary form of arboreal locomotion in an of rodent (Orkin and Pontzer, 2011), carnivoran animal without other morphological specializations for using a fine branch niche. This model would prove use- (Fabre et al., 2013), marsupial (Lemelin and ful to better understand the origins of arboreal behav- Schmitt, 2007; Shapiro et al., 2014), and nonmam- iors in mammals like primates. In this study, we malian vertebrates including frogs, lizards, and examined if locomotion on these substrates influences birds (Herrel et al., 2013; Sustaita et al., 2013) the mid-diaphyseal cross-sectional geometry of mouse that are effective in this niche without primate- metatarsals. Thirty CD-1/ICR mice were raised in like specializations. For most small mammals, a either arboreal (composed of elevated narrow branches key functional demand of this niche is to counter- of varying orientation) or terrestrial (flat ramps and act lateral instability while balancing above very walkways that are stratified) habitats from weaning narrow horizontal supports. Manual and pedal (21 days) to adulthood (4 months). After experiments, prehension is important in this context because it the hallucal metatarsal (Mt1) and third metatarsal (Mt3) for each individual were isolated and micro-com- makes counterbalancing torques possible to main- puted tomography (micro-CT) scans were obtained to tain above branch postures (Napier, 1967; Cart- calculate mid-shaft cross-sectional area and polar sec- mill, 1974, 1985; Preuschoft et al., 1995; Lemelin tion modulus. Arboreal mice had Mt1s that were signif- and Schmitt, 2007). icantly more robust. Mt3 cross sections were not Evidence from extant (Scandentia) and fossil significantly different between groups. The arboreal (Plesiadapiformes) groups suggest that grasping group also exhibited a significantly greater Mt1/Mt3 with an opposable hallux is a common feature of ratio for both robusticity measures. We conclude that fine branch arboreal taxa even when other (nonpe- the hallucal metatarsal exhibits significant phenotypic dal grasping) specializations seen in primates are plasticity in response to arboreal treatment due to absent (e.g., stereoscopic vision; Bloch et al., habitual locomotion that uses a rudimentary hallucal grasp. Our results support the hypothesis that early 2007). Therefore, one interpretation is that adap- adaptive stages of fine branch arboreality should be tations for hallucal grasping represent an early accompanied by a slightly more robust hallux associ- transitional evolutionary stage toward better ated with the biomechanical demands of this niche. J. exploiting a fine branch niche. Such multistaged Morphol. 276:759–765, 2015. VC 2015 Wiley Periodicals, Inc. evolutionary sequences have been proposed in KEY WORDS: arboreal; foot; hallux; pedal grasping; micro-CT; cross-sectional geometry *Correspondence to: Craig D. Byron, Department of Biology, Mercer University, 1501 Mercer University Drive, Macon, GA 31207. E-mail: [email protected] INTRODUCTION It is commonly recognized that Primates (within Received 17 September 2014; Revised 3 January 2015; Eutheria) represent one of a few adaptive radia- Accepted 24 January 2015. tions (many belonging to the Euarchonta) with Published online 11 March 2015 in specialized appendicular anatomy that yields func- Wiley Online Library (wileyonlinelibrary.com). tional advantages in the terminal branches of DOI 10.1002/jmor.20376 VC 2015 WILEY PERIODICALS, INC. 760 C.D. BYRON ET AL. substrates (Fig. 1). The development of this skill for fine branch arboreality is evident at a cerebral and cerebellar somatotopic level (Byron et al., 2013). The habitual use of hallucal grasping com- mits the mouse to foot postures that place the sub- strate between the first and second digits. In climbing mice, the transverse processes on caudal vertebrae are relatively larger, the talar head angle is relatively lower, the talar head width and height are more uniform, and the talar neck is rel- Fig. 1. Still-frame image of a typical mouse on a horizontal atively shorter (Byron et al., 2011). The talar head branch (i.e., arboreal group). These animals use a pedal grasp is especially pertinent to pedal grasping because with an opposable hallux (see left foot) in coordination with tail its angle relative to the skeletal elements of the motions that counteract lateral instability. more distal regions of the foot (i.e., navicular, ento- cuneiform, and metatarsals) is decreased and this relates to pedal inversion relative to the climbing which a nongrasping, small, clawed euarchonto- substrate. gliran mammal (i.e., Stage 1) transitions to a A similar mechanism for enhanced pedal inver- clawed, pedal grasper like the tree shrew genus sion which helps promote stable above branch Ptilocercus (i.e., Stage 2) before evolving a more quadrupedal postures is reported for some euarch- powerful pedal grasp with a nail-bearing hallux ontans (Szalay and Drawhorn, 1980; Sargis, 2001, like that found in the opossum genus Caluromys 2002). Moreover, earlier studies of lab mice and (i.e., Stage 3; Gebo, 2004; Sargis et al., 2007; You- the rodent genus Peromyscus have emphasized the latos, 2008). Accordingly, it should be possible to role of tail use, increased talar neck angle, and ascertain functional morphological signals in bones first metatarsal morphology in climbing behaviors in the foot related to hallucal grasping perform- (Siegel, 1970; Siegel and Van Meter, 1973; Siegel ance. For example, a hallucal metatarsal (Mt1) and Jones, 1975). Recent work with the harvest with a relatively large peroneal process has been mouse (Micromys minutus; Urbani and Youlatos, suggested to be an adaptation for powerful hallu- 2013) substantiate this approach that early stages cal grasping in primates (e.g., Gebo, 2004). This is of primate evolution can be modeled with living because strepsirrhine primates and tarsiers, tradi- rodent species. By combining tiny-size and secure tionally viewed as capable of strong hallucal hallucal grasping, those authors demonstrate that grasps, have larger peroneal processes compared animals not typically viewed as being specialized to anthropoids that lack this morphology (Gebo, for the fine-branch niche can nevertheless exploit 1986, 1987; Szalay and Dagasto, 1988; Jacobs this habitat to a degree of proficiency that is et al., 2009; Patel et al., 2012; Goodenberger et al., between the hypothesized Stages 2 and 3 of pri- 2015). However, experimental (Boyer et al., 2007; mate evolution. Kingston et al., 2010; Patel et al., 2015) and com- Because the alterations in morphology docu- parative (Jacobs et al., 2009; Goodenberger et al., mented by Byron et al. (2011, 2013) occur within a 2015) studies have made it clear that the presence single generation of mice, they are not considered of a large peroneal process alone is not consistent to be evolutionary adaptations. Instead, morpho- with hallucal grasping abilities in primates. Thus, logical changes in the skeletal, muscular, and the putative transition between hypothetical nervous systems relate to experience-dependent evolutionary Stages 1 and 2 may only be accompa- growth and tissue modeling (nonheritable morpho- nied by very modest specializations in Mt1 logical variance) that is relevant to preprimate- morphology. like climbing ability (i.e., phenotypic plasticity; see An approach to assess possible morphological Stearns, 1989; Scheiner, 1993; Via et al., 1995; changes that may have accompanied an evolution- Buck et al., 2010). The hallux, ankle, and tail mor- ary transition from Stages 1 to 2 is to use an ani- phology in these mice could mimic the earliest mal model system. It has been shown that stage of euarchontan evolution into the fine- standard laboratory rodents as well as the Euro- branched niche. Therefore, relating phenotypic pean Red Squirrel locomote on slender substrates plasticity to morphological adaptations for grasp- with adaptive behaviors that promote stability ing could lead to a better understanding on the (Schmidt and Fischer, 2010, 2011). Recently, Byron evolution of integrated organ systems related to et al. (2009, 2011, 2013) also promoted the use of a the early functional demands of the fine-branch mouse model system that simulates a fine-branch niche. arboreal habitat. This is because pedal (specifically In this study, metatarsals are evaluated
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