The Evolution of Micro-Cursoriality in Mammals

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The Evolution of Micro-Cursoriality in Mammals © 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 1316-1325 doi:10.1242/jeb.095737 RESEARCH ARTICLE The evolution of micro-cursoriality in mammals Barry G. Lovegrove* and Metobor O. Mowoe* ABSTRACT Perissodactyla) in response to the emergence of open landscapes and In this study we report on the evolution of micro-cursoriality, a unique grasslands following the Eocene Thermal Maximum (Janis, 1993; case of cursoriality in mammals smaller than 1 kg. We obtained new Janis and Wilhelm, 1993; Yuanqing et al., 2007; Jardine et al., 2012; running speed and limb morphology data for two species of elephant- Lovegrove, 2012b; Lovegrove and Mowoe, 2013). shrews (Elephantulus spp., Macroscelidae) from Namaqualand, Loosely defined, cursorial mammals are those that run fast. South Africa, which we compared with published data for other However, more explicit definitions of cursoriality remain obscure mammals. Elephantulus maximum running speeds were higher than because locomotor performance is influenced by multiple variables, those of most mammals smaller than 1 kg. Elephantulus also including behaviour, biomechanics, physiology and morphology possess exceptionally high metatarsal:femur ratios (1.07) that are (Taylor et al., 1970; Garland, 1983a; Garland, 1983b; Garland and typically associated with fast unguligrade cursors. Cursoriality evolved Janis, 1993; Stein and Casinos, 1997; Carrano, 1999). In an in the Artiodactyla, Perissodactyla and Carnivora coincident with evaluation of these definition problems, Carrano (Carrano, 1999) global cooling and the replacement of forests with open landscapes argued that ‘…morphology should remain the fundamental basis for in the Oligocene and Miocene. The majority of mammal species, making distinctions between locomotor performance…’. Carrano though, remained non-cursorial, plantigrade and small (<1 kg). The (Carrano, 1999) showed that a morphological continuum between extraordinary running speed and digitigrady of elephant-shrews was ‘cursorial’ and ‘graviportal’ (weight-bearing) locomotion based upon established in the Early Eocene in the earliest macroscelid measures of multiple morphological traits in a principal components Prodiacodon, but was probably inherited from Paleocene, Holarctic analysis provided biologically realistic indices of mammalian stem macroscelids. Micro-cursoriality in macroscelids evolved from locomotor performance. In short, cursorial taxa have longer the plesiomorphic plantigrade foot of the possum-like ancestral metatarsals, more slender limb elements, shorter femora, and a mammal earlier than in other mammalian crown groups. Micro- muscle insertion point located closer to the hip joint, whereas cursoriality evolved first in forests, presumably in response to graviportal mammals have more robust limb elements, shorter selection for rapid running speeds facilitated by local knowledge, in metatarsals, and more distal muscle insertion points (Carrano, 1999). order to avoid predators. During the Miocene, micro-cursoriality was Variations in the dimensions of these traits are borne in limbs pre-adaptive to open, arid habitats, and became more derived in the commonly associated with cursoriality, namely the derived newly evolved Elephantulus and Macroscelides elephant-shrews with digitigrade and unguligrade limbs, in which the metatarsals, in trail running. particular, are elongated relative to other hindlimb bones, resulting in the heel being raised off the ground (Hildebrand, 1974; Garland KEY WORDS: Elephant-shrews, Macroscelidae, Running speed, and Janis, 1993). The length ratio between the metatarsals (MT) and Cursors, Mammals the femur (F), the MT:F ratio, is often used as a proxy for cursoriality in mammals (Garland and Janis, 1993; Carrano, 1999). INTRODUCTION Although higher MT:F ratios are often associated with increased The extraordinary diversity of modern placental mammals evolved hindlimb length, stride length and running speed (Hildebrand, 1974), from a single lineage that survived the asteroid impact event that they are also indicative of more specialized limb adaptations for fast drove the non-neornithean dinosaurs to extinction at the running speeds (Steudel and Beattie, 1993) and cost-effective long- Cretaceous–Paleogene (K–Pg) boundary 65.5 million years ago distance locomotion (Garland and Janis, 1993). Nevertheless, there (MYA) (O’Leary et al., 2013). The ancestral placental mammal was is no direct relationship between MT:F ratio and maximum running a small (6–245 g), insectivorous, tree-climbing (scansorial) forest- speed; two mammals with similar body sizes can have similar dweller that looked somewhat like an opossum with a bushy tail maximum running speeds but very different MT:F ratios (Garland (O’Leary et al., 2013). The reconstruction of this virtual placental and Janis, 1993). MT:F ratios range from <0.1 in some plantigrade mammalian ancestor shows the ancestral condition of a plantigrade rodents to 1.4 in the giraffe (Carrano, 1999). foot, in which the heel makes contact with the ground (O’Leary et al., Several published observations on the morphology and 2013). From this ancestor, and given the freedom to radiate into niches physiology of elephant-shrews or sengis (Macroscelidea) prompted evacuated by the non-neornithean dinosaurs, the first members of the us to test the hypothesis that elephant-shrews are exceptional micro- modern placental mammals emerged within hundreds of thousands of cursorial animals relative to typical cursorial taxa. Elephant-shrews years of the extinction event (O’Leary et al., 2013). During the are placed in the superorder Afrotheria (Springer et al., 1997) as a Oligocene and Miocene, a high degree of cursoriality evolved in sister family to Afrosoricida (tenrecs, golden moles and otter several modern placental orders (Carnivora, Artiodactyla and shrews) (Stanhope et al., 1998). The etymology of Macroscelidea confirms the early recognition of unusual hind limb morphology School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville because the word is derived from Macroscelides, which comprises 3209, South Africa. the Latin prefix ‘macro’, meaning large, and the Greek word ‘skelis’, meaning hip or thigh. Indeed, elephant-shrews that have *Authors for correspondence ([email protected]; [email protected]) been studied morphologically to date display extremely elongated Received 12 August 2013; Accepted 5 December 2013 metatarsals and distal muscle reductions (Evans, 1942; Carrano, The Journal of Experimental Biology 1316 RESEARCH ARTICLE The Journal of Experimental Biology (2014) doi:10.1242/jeb.095737 Table 1. Bone dimensions and maximum running speeds of List of symbols and abbreviations Elephantulus rupestris and E. edwardii AIC Akaike’s information criterion CI confidence interval E. rupestris E. edwardii F femur Body mass (g) 60.10±5.02 (n=10) 49.90±4.22 (n=4) K–Pg Cretaceous–Paleogene boundary Femur length (mm) 26.54±0.69 (n=5) 26.13±0.38 (n=5) M body mass b Metatarsal length (mm) 26.68±1.15 (n=5) 24.54±1.26 (n=5) ML maximum likelihood MT:F ratio 1.067±0.041 (n=5) 1.075±0.042 (n=5) MRS maximum running speed (km h−1) MRS (km h−1) 23.6±4.8 (n=10) 19.4±2.2 (n=4) MT metatarsal MRS range (km h−1) 14.4–28.8 10.8–21.6 MT:F metatarsal:femur ratio OLS ordinary least squares MRS, maximum absolute running speed; MT:F, metatarsal:femur. PGLS phylogenetic generalized least squares RRS relative running speed (body lengths s−1) −1 Tb body temperature (°C) body lengths s and Mb) were regressed against each other (Iriarte- Díaz, 2002). Consequently, we resorted here to analyses of MRS only, 1999). Moreover, whereas their closest relatives, tenrecs using a phylogenetically informed approach. (Tenrecidae) and golden moles (Chrysochloridae), display a mean In this study we measured the running speeds and limb body temperature (Tb) of 32.8°C (n=8 species), the mean Tb of morphology of two species of rock elephant-shrew, Elephantulus elephant-shrews is 37.2°C (n=8 species), indicating a profound edwardii (Smith 1839) and E. rupestris (Smith 1831), from apomorphy (derived characteristic) of 4.4°C between sister Namaqualand, South Africa. We recorded the MT:F ratio and Afrotherians (Lovegrove, 2012a; Lovegrove, 2012b) (see maximal running speed (km h−1) and compared these data with supplementary material Fig. S1). High body temperatures are appropriate mammal models for which running speed and MT:F correlated with the MT:F ratio in other cursors (Lovegrove, 2012b), data were available. We tested the hypothesis that elephant-shrews and are thought to enhance muscle performance (Clarke and Pörtner, display a micro-cursorial capacity which evolved in forest 2010). Elephant-shrews also display an exceptionally high MT:F environments with some surety during the Early Eocene, but ratio for their body size, comparable to those of the fastest possibly as early as the Paleocene. unguligrade cursors (Lovegrove, 2012b). Last, elephant-shrews (Elephantulus) displayed the highest index of cursoriality in a RESULTS principal components analysis of mammal limb dimensions Metatarsal:femur ratios (Carrano, 1999). The average MT:F ratio of the two species of Elephantulus was 1.07 The extraordinary large hind limbs/quarters and speed of (Table 1). Excluding the giraffe, only five mammals in the combined elephant-shrews were also recognized in the very first written dataset of 135 mammals had MT:F ratios higher than those of E. description of these African small mammals in
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