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Variability and Constraint of Vertebral Formulae and Proportions In Folia Morphol. Vol. 77, No. 1, pp. 44–56 DOI: 10.5603/FM.a2017.0064 O R I G I N A L A R T I C L E Copyright © 2018 Via Medica ISSN 0015–5659 www.fm.viamedica.pl Variability and constraint of vertebral formulae and proportions in colugos, tree shrews, and rodents, with special reference to vertebral modification by aerodynamic adaptation T. Kawashima1, R.W. Thorington Jr.2, P.W. Bohaska2, F. Sato1 1Department of Anatomy, School of Medicine, Toho University, Tokyo, Japan 2Department of Vertebrae Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, United States [Received: 4 April 2017; Accepted: 19 June 2017] Background: The aim of the present study is to provide the first large data set on vertebral formulae and proportions, and examine their relationship with different locomotive modes in colugos (Dermoptera), tree shrews (Scandentia), and rodents (Rodentia), which have been considered less variable because they were thought to have a plesiomorphic number of 19 thoracolumbar vertebrae. Materials and methods: The data included 33 colugos and 112 tree shrews, which are phylogenetically sister taxa, and 288 additional skeletons from 29 other mammalian species adapted to different locomotive modes, flying, gliding, arboreal, terrestrial, digging, and semi-aquatic habitats. Results: The following results were obtained: (1) intra-/interspecies variability and geographical variation in thoracic, lumbar, and thoracolumbar counts were pre- sent in two gliding colugo species and 12 terrestrial/arboreal tree shrew species; (2) in our examined mammals, some aerodynamic mammals, such as colugos, southern flying squirrels, scaly-tailed squirrels, and bats, showed exceptionally high amounts of intraspecific variation of thoracic, lumbar, and thoracolumbar counts, and sugar gliders and some semi-aquatic rodents also showed some variation; (3) longer thoracic and shorter lumbar vertebrae were typically shared traits among the examined mammals, except for flying squirrels (Pteromyini) and scaly-tailed squirrels (Anomaluridae). Conclusions: Our study reveals that aerodynamic adaptation could potentially lead to strong selection and modification of vertebral formulae and/or proportions based on locomotive mode despite evolutionary and developmental constraints. (Folia Morphol 2018; 77, 1: 44–56) Key words: colugo, tree shrew, aerodynamic mammals, vertebral column, gliding adaptation INTRODUCTION using classical descriptive data by Owen [38]; they Narita and Kuratani [33] provided developmental concluded that 19 thoracolumbar (TL) vertebrae in understanding of mammalian axial vertebral formulae many mammalian groups tend to be fixed because Address for correspondence: Dr. T. Kawashima, Department of Anatomy, School of Medicine, Toho University. 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan, tel: +81-3-3762-4151, fax: +81-3-5493-5411, e-mail: [email protected] 44 T. Kawashima et al., Vertebral changes in aerodynamic mammals of developmental constraints, as seen in a stable ships among axial vertebral counts and proportions, cervical count of 7; however, most Carnivora have lineage-specific developmental constraints, and/or 20 TL vertebrae, which shows a lineage-specific pat- functional adaptation by different locomotive modes. tern. Because of the limited sample size in Owen’s catalogue [38], to obtain more accurate conclusions MATERIALS AND METHODS it is necessary to examine a larger sample size, as in Materials used some studies [1, 39, 41, 54, 55, 62]. In total, 433 postcranial skeletons were used for Asher et al. [2] conducted a statistical analysis on this study, as listed in Table 1. mammalian vertebral formulae using a larger sam- As the main materials, the vertebral formulae and ple size and concluded that xenarthrans and afroth- proportions of 33 colugos (or flying lemurs; Dermop- erians have a high proportion of individuals with tera) and 112 tree shrews (Scandentia) were intensively meristic deviation from species’ median counts, and examined from dry skeletons to assess their morpho- monotremes, xenarthrans, afrotherians, and primates logical similarities and differences, because they are have relatively high variation in TL count [2]. The phylogenetically sister taxa. extreme vertebral formulae in some mammals, such Furthermore, an additional 288 postcranial skel- as afrotherians and xenarthrans, have recently been etons from 29 mammalian specimens of 16 rodent, thoroughly re-examined [7, 23, 42]. bat, and marsupials (sub-) families that include all Alternatively, it is well known that rodents are other aerodynamic mammals were compared to the least variable mammals and are thought to have test the hypothesis that morphological changes of a fixed TL count of 19 without any deviations [2, 42]. vertebral formula and proportion differ based on However, they live in a wide variety of habitats, such locomotive mode. Any individuals with pathological as air, trees, land, water, and soil; additionally, they abnormalities were excluded from this study. represent 38% of mammal species [10]. To identify the lineage-specific trend in TL counts of rodents, various Identification and measurement of vertebrae rodents should be examined, from frequently used For identification of each vertebra, the vertebral experimental rodents to uniquely specialised rodents, morphology was considered the most important cri- such as gliding scaly-tailed squirrels (Anomalidae) and terion, as in other studies [2, 40]. burrowing pocket gophers (Geomyodae), which have Thoracic vertebrae were principally identified as not been previously studied. those elements with rib facets on or near the verte- In our past research on colugos [27, 28], we found bral neural arch, or the presence of articulated ribs. that there was insufficient data regarding colugo In addition, anatomical characteristics were usually anatomy compared with other mammals. Colugos, present, such as species-dependent morphology of arboreal and nocturnal mammals with a specialised the shape, size, width, height, and angle of the ver- ability to glide, tend to evade capture [31]. There are tebral body, and transverse and spinous processes therefore limited specimens available for research. with lumbar vertebrae (Fig. 1A, B). We tested the hypothesis that axial vertebrae If there were difficulties with identification of short adapt to different locomotive modes, and are modi- unarticulated ribs or long lumbar transverse processes fied despite evolutionary and developmental con- (Fig. 1C), thoracic and lumbar vertebrae were identi- straints, using some of the perceived least variable fied based on the above anatomical characteristics; mammals with regard to thoracolumbar count (fixed the thoracic vertebrae were generally more slender at 19), including colugos, tree shrews, and rodents. and weaker than lumbar vertebrae [40], although The aims of the present study are to (1) provide these vertebral characteristics differ by species. the first large data set on vertebral formulae and Lumbar vertebrae were identified as those ele- proportions in colugos and tree shrews, which are ments cranial to the sacro-iliac articulation lacking sister taxa; (2) compare these data with those of ro- conspicuous rib facets and showing a transverse pro- dents adapted to different locomotive modes, such as cess (Fig. 1D). Some difficult cases, in which the most those that are gliding/arboreal, terrestrial, digging, or caudal lumbar vertebra partially fused into sacral semi-aquatic, and include all five aerodynamic mam- vertebrae as one sacral bone and articulated with mals: colugos, flying squirrels, scaly-tailed squirrels, the iliac bone, were defined based on anatomical sugar gliders, and bats; and (3) elucidate the relation- characteristics. 45 Folia Morphol., 2018, Vol. 77, No. 1 +12;5 G1<9=54<1C5A91;B +12;5 G1<9=54<1C5A91;B+12;5 G1<9=54<1C5A91;B Table 1. Examined materials *?5395B 129C1CB $>3><>C9E5<>45B *1<?;5B9I5 !=BC9CDC9>= +12;5 G1<9=54<1C5A91;B *?5395B*?5395B 129C1CB $>3><>C9E5<>45B 129C1CB $>3><>C9E5<>45B*1<?;5B9I5*1<?;5B9I5 !=BC9CDC9>=!=BC9CDC9>= +12;5 G1<9=54<1C5A91;B>;D7>B>A;H9=7;5<DAB'A45A5A<>?C5A1 +12;5 G1<9=54<1C5A91;B+12;5 G1<9=54<1C5A91;B>;D>7;>DB7>>BA>A;H9=;H79=;57<;5D<ABDAB'A'45A4A5A5A<5A><?>C5?AC15A1 *?5395B 129C1CB $>3><>C9E5<>45B *1<?;5B9I5 !=BC9CDC9>=!=BC9CDC9>= Species+12;5 G1<9=54<1C5A91;B+12;5 G1<9=54<1C5A91;B *?5395B 129C1CB $>3><>C9E5<>45BHabitats/Locomotive modes*1<?;5B9I5 Sample !=BC9CDC9>=Institution** +12;5 G1<9=54<1C5A91;B+12;5 G1<9=54<1C5A91;B>;D0 #"/ /$%&"70 #"/ /$%&">B>A;H9=7;5<DAB'A45A5A<>?C5A1 *?5395B 129C1CB $>3><>C9E5<>45B *1<?;5B9I5 !=BC9CDC9>= >;;D7>0 #"/ /$%&"B>AA;;H99=7;;5<DAAB'AA45AA5AA<>?CC5AA1 *?5395B*?5395B 129C1CB $>3><>C9E5<>45B129C1CB $>3><>C9E5<>45B *1<?;5B9I5*1<?;5B9I5 size !=BC9CDC9>=!=BC9CDC9>= +12;5 G1<9=54<1C5A91;B>;D7>B>A;H9=7;5<D(89;9??9=53>;D7>AB'A45A5A<>? /$%&"+),%"$)C5A1 *?5395B*?5395B ;949=7 129C1CB $>3><>C9E5<>45B129C1CB $>3><>C9E5<>45B 1=79=7 A2>A51; *1<?;5B9I5*1<?;5B9I5 ,*&% %& %% %' ,%0 % %&!=BC9CDC9>=!=BC9CDC9>= & +12;5 G1<9=54<1C5A91;B>;D70 #"/ /$%&">B>A;H9=7;5<(89;9??9=53>;D7>DA(89;9??9=53>;D7>B'A45A5A<>? /$%&"+),%"$)C5 /$%&"+),%"$)A1 *?5395B ;949=7 129C1CB $>3><>C9E5<>45B;949=7 1=79=7 A2>A51; 1=79=7 A2>A51; *1<?;5B9I5 ,*&% %&,*&% %& %% %' ,%0 % %& %% %' ,%0 % %&!=BC9CDC9>= & & +12;5 G1<9=54<1C5A91;B>>;D;D77>0 #"/ /$%&">BB>>AA;H;H9=9=77;5;5<<DDAABB''AA4455AA55AA<<>>??CC55AA11 Colugos>>;D;D77>>B orB>> AFlyingA;H;H9=9=7 7lemurs;5;5<<DD*D=413>;D7>AABB (Order''AA4455AA Dermoptera55AA<<
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