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Perissodactyla: Tapirus**) Exposed Using Geometric Morphometrics

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Perissodactyla: Tapirus**) Exposed Using Geometric Morphometrics This item is the archived peer-reviewed author-version of: Interspecific variation in the tetradactyl manus of modern tapirs (**Perissodactyla: Tapirus**) exposed using geometric morphometrics Reference: Maclaren Jamie, Nauw elaerts Sandra.- Interspecific variation in the tetradactyl manus of modern tapirs (**Perissodactyla: Tapirus**) exposed using geometric morphometrics Journal of morphology - ISSN 0362-2525 - 278:11(2017), p. 1517-1535 Full text (Publisher's DOI): https://doi.org/10.1002/JMOR.20728 To cite this reference: https://hdl.handle.net/10067/1455380151162165141 Institutional repository IRUA Page 1 of 53 Journal of Morphology MacLaren 1 1 2 3 1 Interspecific variation in the tetradactyl manus of modern tapirs 4 5 6 2 (Perissodactyla: Tapirus) exposed using geometric morphometrics 7 8 9 1 1 & 2 10 3 Authors: Jamie A. MacLaren * and Sandra Nauwelaerts 11 12 4 13 14 15 5 Affiliation: 16 17 18 6 1 Department of Biology,For Universiteit Peer Antwerpen, BuilReviewding D, Campus Drie Eiken, 19 20 7 Universiteitsplein, Wilrijk, Antwerp, 2610, Belgium 21 22 23 8 2 Centre for Research and Conservation, Koninklijke Maatschappij voor Dierkunde (KMDA), 24 25 9 Koningin Astridplein 26, Antwerp, 2018, Belgium 26 27 28 10 29 30 31 11 * Corresponding author 32 33 34 12 35 36 37 13 Corresponding Author: Jamie A. MacLaren, Room D1.41, Building D, Campus Drie Eiken, 38 39 14 Universiteitsplein 1, 2610 Antwerp, Belgium 40 41 42 15 Correspondence Email: [email protected] 43 44 45 16 Correspondence Telephone: (+32) 32 65 1994 46 47 48 17 49 50 51 18 52 53 54 19 Short Title: Shape variation in the tapir manus 55 56 20 57 58 59 60 John Wiley & Sons Journal of Morphology Page 2 of 53 MacLaren 2 1 2 3 21 Abstract 4 5 6 22 The distal forelimb (autopodium) of quadrupedal mammals is a key morphological unit involved in 7 8 23 locomotion, body support and interaction with the substrate. The manus of the tapir (Perissodactyla: 9 10 24 Tapirus ) is unique within modern perissodactyls, as it retains the plesiomorphic tetradactyl (four- 11 12 13 25 toed) condition also exhibited by basal equids and rhinoceroses. Tapirs are known to exhibit 14 15 26 anatomical mesaxonic symmetry in the manus, although interspecific differences and biomechanical 16 17 27 mesaxony has yet to be rigorously tested . Here, we investigate variation in the manus morphology of 18 For Peer Review 19 28 four modern tapir species ( Tapirus indicus , T. bairdii , T. pinchaque and T. terrestris ) using a 20 21 29 geometric morphometric approach . Autopodial bones were laser scanned to capture surface shape 22 23 24 30 and morphology was quantified using 3D landmark analysis. Landmarks were aligned using 25 26 31 Generalised Procrustes Analysis, with discriminant function and partial least square analyses 27 28 32 performed on aligned coordinate data to identify features that significantly separate tapir species. 29 30 33 Overall, our results support the previously held hypothesis that T. indicus is morphologically 31 32 33 34 separate from neotropical tapirs; however, previous conclusions regarding function from 34 35 35 morphological differences are shown to require reassessment. We find evidence indicating that T. 36 37 36 bairdii exhibits reduced reliance on the lateral fifth digit compared to other tapirs. Morphometric 38 39 37 assessment of the metacarpophalangeal joint and the morphology of the distal facets of the lunate 40 41 38 lend evidence towards not only high loading on the lateral digits of both the large T. indicus (large 42 43 44 39 body mass) and the small , long limbed T. pinchaque (ground impact). Our results support other 45 46 40 recent studies on T. pinchaque , suggesting subtle but important adaptations to a compliant but 47 48 41 inclined habitat. In conclusion, we demonstrate further evidence that the modern tapir forelimb is a 49 50 42 variable locomotor unit with a range of interspecific features tailored to habitual and biomechanical 51 52 53 43 needs of each species. 54 55 44 Keywords:- discriminant function – locomotion – manus – mesaxonic symmetry – tetradactyl 56 57 58 59 60 John Wiley & Sons Page 3 of 53 Journal of Morphology MacLaren 3 1 2 3 45 Introduction 4 5 6 46 Modern tapirs (Tapiridae; Tapirus Brünnich) are enigmatic, forest-dwelling representatives of the 7 8 47 order Perissodactyla (odd-toed ungulates) (Steiner & Ryder 2011; Cozzuol et al. 2013; Ruiz-García 9 10 48 et al. 2012). In addition to equids (horses, asses and zebras) and rhinoceroses, tapirs represent the last 11 12 13 49 members of a formerly highly speciose order of small to very large herbivores (Norman & Ashley 14 15 50 2000; Janis 1989). The tetradactyl (four-toed) manus of the modern tapir is a unique feature in extant 16 17 51 perissodactyls, with equids and rhinoceroses having reduced their functional digit number to one and 18 For Peer Review 19 52 three respectively (MacFadden 1992); the earliest ancestors of rhinoceroses, tapirs and equids also 20 21 53 displayed a tetradacyl manus (Holbrook 2001). The small, basal members of the Perissodactyla (e.g. 22 23 24 54 Propalaeotherium , Hyracotherium , Heptodon ) are interpreted as forest-dwelling browsers with a 25 26 55 ‘primitive’ digital condition, bearing three toes on the hind foot (tridactyly) and four on the forefoot 27 28 56 (Hellmund 2005; Wood et al. 2010; Radinsky 1965; Holbrook 2001). This plesiomorphic 29 30 57 characteristic of the tapir manus, among other features of tapir anatomy, has contributed to the 31 32 33 58 traditional interpretation of tapirs as ‘living fossils’ (Janis 1984; Hershkovitz 1954; Padilla et al. 34 35 59 2010; Schoch 1989). Consequently, extant tapirs have been the object of numerous morphological 36 37 60 and ecological comparisons to extinct tetradactyl perissodactyls (including Radinsky 1965; Janis 38 39 61 1984; Holbrook 2001, 2009). However, these studies often treat Tapirus either as a single 40 41 62 morphological unit (e.g. Holbrook 1999, 2001), or compare only one or two species of Tapirus with 42 43 44 63 extinct tetradactyl perissodactyls (e.g. Simpson 1945; Radinsky 1965). Recent studies on the extinct 45 46 64 tapirs of North America are beginning to increase species counts when performing comparative 47 48 65 analyses, albeit with predominantly qualitative techniques (Hulbert 1995; Hulbert 2005; Hulbert 49 50 66 2010; Hulbert et al. 2009; Holanda et al. 2012). Using Tapirus as a solitary morphological unit is 51 52 53 67 greatly beneficial for phylogenetic comparisons with more basal tapiromorph perissodactyls, e.g. 54 55 68 Lophiodon (Holbrook 2009) and Colodon (Colbert 2005), as it does not require exhaustive character 56 57 69 comparisons across all species of tapir through time. However, to test evolutionary questions on the 58 59 60 John Wiley & Sons Journal of Morphology Page 4 of 53 MacLaren 4 1 2 3 70 functional morphology of the postcranial skeleton in basal, tetradactyl perissodactyls, a 4 5 71 comprehensive understanding of limb variation in potential modern analogues is essential. One such 6 7 72 question concerns the true axis of symmetry in the mesaxonic autopodium. 8 9 10 73 11 12 13 74 Perissodactyls, including tetradactyl, tridactyl and monodactyl taxa, possess mesaxonic symmetry in 14 15 75 their manus (Klaits 1971); the axis of symmetry passes through the third digit. The term ‘mesaxonic’ 16 17 18 76 has been used to describeFor autopodia Peer in a variety of tetrapodReview groups. Anatomical and morphometric 19 20 77 studies determine a mesaxonic autopodium to exhibit a third digit that is longer than all the others, 21 22 78 flanked by digits two and four, which are shorter than digit three but of comparable length to one 23 24 79 another (Reghem et al. 2012; Lockley 2009; Brown & Yalden 1973; Tougard et al. 2001; Rajkumar 25 26 27 80 & Klein 2014). Other studies approach the subject of mesaxony from a more functional and 28 29 81 biomechanical standpoint, suggesting that mesaxonic symmetry is not exclusively defined by longer 30 31 82 third digits, but that the central third digit is loaded most greatly during locomotion . Lateral digits are 32 33 83 then loaded approximately equally (Brown & Yalden 1973; Klaits 1971; Holbrook 2001), with the 34 35 84 third digit acting as the centre of rotation during lift-off of the foot (Klaits 1971). The first, 36 37 38 85 anatomical definition of mesaxonic symmetry has been known to be true for perissodactyls for many 39 40 86 years (Earle 1893; Earle 1896; Simpson 1945; Gregory 1929); the second, biomechanical 41 42 87 interpretation has yet to be explored in all living perissodactyl groups. Understanding the 43 44 88 comparative morphology of the manus in modern tapirs, which are known to exhibit anatomical 45 46 47 89 mesaxonic symmetry, may reveal osteological evidence for variation in load application across the 48 49 90 four manual digits that also support the biomechanical interpretation of mesaxonic symmetry. 50 51 91 Unfortunately the majority of tapir postcranial research has centred on qualitative descriptions, with 52 53 92 little by way of quantitative morphological investigation required for proper functional 54 55 93 interpretations. 56 57 58 59 60 John Wiley & Sons Page 5 of 53 Journal of Morphology MacLaren 5 1 2 3 94 4 5 6 95 Previous qualitative studies of modern tapir postcranial morphology have revealed interspecific 7 8 96 differences, almost exclusively between the lowland tapir ( T. terrestris L.) and the Malayan tapir ( T. 9 10 97 indicus Desmarest) (Earle 1893; Gregory 1929) . Results often align, with T. indicus shown to 11 12 13 98 possess longer, heavier and more graviportally adapted limb elements compared to T. terrestris in all 14 15 99 analyses (Earle 1893; Osborn 1929; Hulbert 1995).
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