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Evolution of Bone Cortical Compactness in Slow Arboreal Mammals

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Evolution of Bone Cortical Compactness in Slow Arboreal Mammals bioRxiv preprint doi: https://doi.org/10.1101/2020.09.02.279836; this version posted September 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Evolution of bone cortical compactness in slow arboreal mammals 2 3 Alfieri F.1,2, Nyakatura J.A.1, Amson E.2 4 1. Institut für Biologie, Humboldt Universität zu Berlin, Berlin, Germany. 5 6 2. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, 7 Germany. 8 9 10 Abstract 11 Lifestyle convergences and related phenotypes are a major topic in evolutionary biology. Low bone 12 cortical compactness (CC), shared by the two genera of ‘tree sloths’, has been linked to their convergently 13 evolved slow arboreal ecology. The proposed relationship of low CC with ‘tree sloths’ lifestyle suggests a 14 potential convergent acquisition of this trait in other slow arboreal mammals. ‘Tree sloths’, ‘Lorisidae’, 15 Palaeopropithecidae, Megaladapis and koalas were included in a phylogenetically informed CC analysis of 16 the humerus and femur, as well as closely related but ecologically distinct taxa. We found that ‘tree sloths’ are 17 unparalleled by any analysed clade, in featuring an extremely low CC. A tendency for low CC was however 18 found in palaeopropithecids (especially Palaeopropithecus) and Megaladapis. On the other hand, low CC was 19 not found in ‘Lorisidae’. Koalas, although deviating from the compact structure generally observed in 20 mammals, are not clearly distinct from their sister taxon (wombats) and show humeral CC that is higher than 21 femoral CC. Multiple factors seem to influence CC, preventing the recognition of a simple relationship 22 between slow arborealism and low CC. Highly compact cortical bone in extinct sloths confirms that low CC 23 in ‘tree sloths’ likely represents a recent convergence. 24 25 Corresponding author: Fabio Alfieri, email: [email protected] 26 27 Keywords: convergent evolution, bone microstructure, humerus, femur, tree sloths, subfossil lemurs bioRxiv preprint doi: https://doi.org/10.1101/2020.09.02.279836; this version posted September 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 28 1. Background 29 Tetrapod long bones microstructure is known to reflect life history, physiology, phylogeny, ontogenetic 30 growth and lifestyle [1–3]. Indeed, diaphyseal microstructure has been related to ecology [2,4,5] and employed 31 to infer it in extinct tetrapods (e.g. [6,7]). Moreover, this relationship potentially enables to recognise patterns 32 of convergent evolution [8]. 33 To highlight convergent phenotypes, mammals are particularly suitable to be investigated given their 34 remarkable diversity of lifestyles. Mammalian groups with different ecological adaptations can be 35 discriminated analyzing several diaphyseal microstructural parameters (e.g. [9,10]). The amount of porosities 36 in the diaphyseal compact cortical bone, or cortical compactness (CC), was recently quantified in the humerus 37 of adult extant and extinct xenarthrans. The two lineages of extant sloths (Choloepus and Bradypus), 38 characterised by an exceptionally slow arboreal lifestyle [11], were found to feature lower CC in respect to 39 other similar-sized taxa which conversely follow the generalised mammalian condition of high CC [12]. 40 Because ‘tree sloths’ are not monophyletic (hence the quotation marks employed herein), this trait was 41 identified as one of the convergent traits related to their independently acquired slow arboreal lifestyle [11,12]. 42 If indeed driven by adaptation to this lifestyle, a low CC may have convergently evolved in other slow arboreal 43 therians, too. With ‘Slow Arboreal’, we refer to species characterised by exceptionally slow and cautious 44 movements on trees and daily activities budgets dominated by rest and quiescence. This set of traits is generally 45 associated with unusually low metabolic rate. To date, no CC analyses were performed on slow arboreal 46 mammals, beside the one on ‘tree sloths’ [12]. Following the latter, we quantified CC in the humerus. 47 Moreover, we also investigated CC of the femur, since this bone is often employed in microstructural analysis 48 (e.g. [13,14]). 49 Together with ‘tree sloths’, we analysed other known slow arboreal lineages, namely the koala 50 Phascolarctos cinereus [15] and ‘lorisids’ [16], with the latter arguably representing a paraphyletic group (see 51 Materials and Methods). Moreover, taxa from two late Quaternary-Holocene subfossil lineages of Malagasy 52 strepsirrhines, Palaeopropithecidae (Palaeopropithecus, Mesopropithecus and Babakotia) and Megaladapidae 53 (Megaladapis) [17,18], are here investigated. They were described as slow and poorly agile arboreal, through 54 postcranial (gross anatomy, e.g. [17,19], diaphyseal and epiphyseal geometric properties, [20]) and cranial [21] bioRxiv preprint doi: https://doi.org/10.1101/2020.09.02.279836; this version posted September 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 55 evidences (reviewed in [18,20]). Beside the taxa introduced above, a set of close relatives, conversely 56 characterised by different lifestyles, is also studied (Figure 1, Table S1). Taking into account phylogenetic 57 relationships, this ecologically heterogeneous sample enables to identify convergent acquisitions of slow 58 arboreality in the sampled taxa and to highlight a potential pattern of convergent low CC in slow arboreal 59 therians. Noticeably, the sample characterised by distinct lifestyles includes specimens of extinct sloths from 60 the Patagonian Early Miocene Santa Cruz Formation [22–24]. Analyzing them can additionally inform on the 61 evolution of low CC in the two lineages of ‘tree sloths’ and corroborate the proposed recent convergence [12]. 62 In this study, humeral and femoral CC are quantified in a wide mammalian sample, representing slow 63 arboreal clades and near relatives with diverging lifestyles. Results are interpreted in a phylogenetically 64 informed manner. In this way, slow arboreality convergences could be reconstructed and ecological effects on 65 CC are preponderantly taken into account. If a direct relationship with this extreme lifestyle is present, we 66 expect to find the convergent slow arboreal groups consistently showing lower CC in respect to close relatives. 67 68 2. Material and Methods 69 70 a. Sampled collections 71 Ten mammals collections were sampled: Museum für Naturkunde, Berlin (ZMB), Staatliches Museum 72 für Naturkunde, Stuttgart (SMNS), Zoologisches Forschungsmuseum Alexander Koenig, Bonn (ZFMK), 73 Zoologische Staatssammlung, Munich (ZSM), Germany; Naturhistorisches Museum, Wien (NMW), Austria; 74 Muséum national d'Histoire naturelle, Paris (MNHN), France; American Museum of Natural History, New 75 York, NY, (AMNH), Field Museum of Natural History, Chicago, IL, (FMNH), Yale Peabody Museum of 76 Natural History, New Haven, CT, (YPM-PU) and Division of Fossil Primates, Duke Lemur Center, Durham. 77 NC (DPC), USA. A total of 106 humeri and 106 femora, belonging to 47 taxa were sampled. Only non- 78 pathological, non-captive and adult individuals were included. Adulthood was established assessing the degree 79 of epiphyseal fusion, in general, and bone size for marsupials, given their incomplete epiphyseal fusion through 80 adulthood [25]. bioRxiv preprint doi: https://doi.org/10.1101/2020.09.02.279836; this version posted September 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 81 82 Figure 1. Time-calibrated tree of mammalian taxa here analysed. Six events of convergent acquisition of ‘Slow Arboreal’ 83 adaptations were reconstructed with Stochastic Character Mapping [26]. It is shown by light blue branches and rectangles. 84 Taxa not sampled for the cortical compactness analysis are indicated with *. The figure was built with the ‘geoscalePhylo’ 85 function (‘strap’ R 3.6.3. package, [27]) and modified in Inkscape [28]. 86 87 b. Data acquisition 88 Bones were scanned using micro Computed-Tomography (µCT) (Phoenix | x-ray Nanotom, GE Sensing 89 and Inspection Technologies GmbH; XYLON FF35-CT-System, YXLON GmbH; Microtomograph RX 90 EasyTom 150; Nikon XTH 225 ST; GE v|tome|x). CC being acquired at mid-diaphysis (see below), the field 91 of CT-scan acquisition was focused on this region, in order to reach the highest possible resolution. The mid- 92 shaft was defined as 50% of the whole bone length (Figure S1). Image stacks (16-bit tifs) were acquired with 93 a resolution ranging from 0.0045 to 0.0662 mm (Table S2 and S3), from which the 50% slice was taken. This 94 resolution range typically allows capturing all vacuities except for the smaller lumen of osteons [12] and it is bioRxiv preprint doi: https://doi.org/10.1101/2020.09.02.279836; this version posted September 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 95 here confirmed for lower resolutions as well. The resolution is unavoidably affected by interspecific 96 differences in bone gross anatomy. Indeed, the presence of bony processes at mid-diaphysis (e.g. third 97 trochanter in the femur of Cingulata) forces an acquisition with longer specimen to X-ray source distance, thus 98 with lower resolution.
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