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1 Primitive bat from the Early Eocene of Wyoming: flight and the evolution of echolocation Nancy B. Simmons 1, Kevin L. Seymour 2, Jörg Habersetzer 3 & Gregg F. Gunnell 4 1 American Museum of Natural History, Central Park West at 79 th Street, New York, NY 10024, USA 2 Royal Ontario Museum, 100 Queen s Park, Toronto, ON M5S 2C6, Canada 3 Forschungsinstitut Senckenberg, Senckenberganlage 25, D-60325, Frankfurt am Main, Germany 4 Museum of Paleontology, University of Michigan, Ann Arbor, MI , USA 1. Supplementary Tables Supplementary Table 1. Skull and limb measurements of Eocene bats including Onychonycteris finneyi Supplementary Table 2. Aspect Ratio Indices of extant and Eocene fossil bats Supplementary Table 3. Brachial and Intermembral Indices for Eocene bats and selected non-volant taxa 2. Supplementary Figures Supplementary Figure 1. Dentition of holotype of Onychonycteris finneyi Supplementary Figure 2. Close-up view of basicranium of holotype of Onychonycteris finneyi Supplementary Figure 3. Close-up view of foot and calcar of holotype of Onychonycteris finneyi Supplementary Figure 4. Paratype of Onychonycteris finneyi Supplementary Figure 5. Phylogenetic tree of bats based on unconstrained parsimony analysis of morphological data Supplementary Figure 6. Phylogenetic tree of bats based on constrained parsimony analysis (molecular backbone tree) Supplementary Figure 7. Basicranium vs. cochlear width in Pteropodidae, Vespertilionidae, and Eocene bats. 1
2 Supplementary Figure 8. Basicranium vs. cochlear width in Phyllostomidae, Molossidae, Emballonuridae, Hipposideridae, Rhinolophidae, and Mormoopidae. Supplementary Figure 9. Basicranium vs. cochlear width in Megadermatidae, Nycteridae, Natalidae, Rhinopomatidae, Thyropteridae, Mystacinidae, Craseonycteridae, and Noctilionidae. Supplementary Figure 10. Wing form of Onychonycteris compared with other extinct and extant bats 3. Supplementary References 2
3 1. Supplementary Tables Supplementary Table 1. Skull and limb measurements of Eocene bats including Onychonycteris finneyi. MC = metacarpal; PP = proximal phalanx; IP = intermediate phalanx; DP = distal phalanx; ROM = Royal Ontario Museum (Toronto); YPM-PU = Yale Peabody Museum, Princeton University Collection (New Haven); FMNH = Field Museum of Natural History (Chicago); LNK = Landessammlungen für Naturkunde (Karlsruhe); SMF = Forschungsinstitut Senckenberg (Frankfurt am Main); HLMD = Hessiches Landesmuseum (Darmstadt); BE = Institut Royale des Sciences (Brussels). Citations are provided for data taken from the literature; all other measurments were made by the authors. 3
4 Onychonycteris finneyi Specimen ROM 55351A (Holotype) ROM (Cast of Paratype) Skull Body Tail Femur Tibia Humerus Radius Digit I MC I PP I DP I Digit II MC II PP II IP II DP II Digit III MC III PP III IP III DP III Digit IV MC IV PP IV IP IV DP IV Digit V MC V PP V IP V DP V
5 Icaronycteris index Specimen LNK 124/ YPM-PU ROM FMNH PM Skull Body Tail Femur Tibia Humerus Radius Digit I MC I PP I DP I Digit II MC II PP II IP II DP II Digit III MC III PP III IP III DP III Digit IV MC IV PP IV IP IV DP IV Digit V MC V PP V IP V DP V
6 Archaeonycteris trigonodon Specimen SMF Me 963a 11 SMF Me SMF 80/ Skull Body Tail Femur Tibia Humerus Radius Digit I MC I PP I DP I Digit II MC II PP II IP II DP II Digit III MC III PP III IP III DP III Digit IV MC IV PP IV IP IV DP IV Digit V MC V PP V IP V DP V
7 Palaeochiropteryx tupaiodon Palaeochiropteryx spiegeli Specimen SMF Me SMF Me SMF Me HLMD Me 32/29 11 SMF Me Skull Body Tail Femur Tibia Humerus Radius Digit I MC I PP I DP I Digit II MC II PP II IP II DP II Digit III MC III PP III IP III DP III Digit IV MC IV PP IV IP IV DP IV Digit V MC V PP V IP V DP V
8 Hassianycteris messelensis Hassianycteris magna Tachypteron franzeni Specimen SMF Me SMF Me HLMD BE (Holotype) 24 Skull Body Tail Femur Tibia Humerus Radius Digit I MC I PP I DP I Digit II MC II PP II IP II DP II Digit III MC III PP III IP III DP III Digit IV MC IV PP IV IP IV DP IV Digit V MC V PP V IP V DP V
9 Supplementary Table 2. Aspect Ratio Indices (ARI) for Eocene fossil bats with representative values from extant bat families for comparison. ARI = [length of digit III + the length of the radius] / length of digit V. Higher values indicate proportionately longer, narrower wings. Taxon Aspect Ratio Index Data Source Onychonycteris finneyi 1.74 This Paper Icaronycteris index Archaeonycteris trigonodon Palaeochiropteryx tupaiodon Palaeochiropteryx spiegeli Hassianycteris messelensis Hassianycteris magna Tachypteron franzeni Pteropodidae Rhinopomatidae Megadermatidae Rhinolophidae Emballonuridae Nycteridae Noctilionidae Mormoopidae Phyllostomidae
10 Mystacinidae Natalidae Vespertilionidae Miniopterinae Molossidae
11 Supplementary Table 3. Brachial and Intermembral Indices for Eocene bats and selected non-volant taxa. UM = University of Michigan Museum of Paleontology; UMMZ = University of Michigan Museum of Zoology. Specimen Taxon Brachial Intermembral ROM 55351A Onychonycteris finneyi ROM Onychonycteris finneyi LNK 124/126 Icaronycteris index YPM-PU Icaronycteris index ROM Icaronycteris index FM PM Icaronycteris index SMF Me 963a Archaeonycteris trigonodon SMF Me 663 Archaeonycteris trigonodon SMF 80/1379 Archaeonycteris trigonodon SMF Me 207 Palaeochiropteryx tupaiodon SMF Me 1032 Palaeochiropteryx tupaiodon HLMD Me 32/29 Palaeochiropteryx spiegeli SMF Me 1008 Palaeochiropteryx spiegeli SMF Me 1469 Hassianycteris messelensis SMF Me 492 Hassianycteris messelensis HLMD 7539 Hassianycteris magna BE Tachypteron franzeni UMMZ Choloepus hoffmanni UMMZ Bradypus variegatus Tupaia glis Ptilocercus lowii FMNH Cynocephalus volans
12 UMMZ Glaucomys volans UMMZ Sciurus niger UMMZ Eutamias quadrivittatus UMMZ Cynomys ludovicianus UMMZ Spermophilus columbianus UMMZ Lynx rufus UM R1605 Procyon lotor
13 2. Supplementary Figures Supplementary Figure 1. Dentition of Onychonycteris finneyi (ROM 55351A, holotype skull, ventral view). Lower and upper jaws are in tight occlusion. Dental features that are evident include: primitive chiropteran dental formula of / ; tribosphenic dentition with dilambdodont upper molars; I1 smaller than I2 with I2 being nearly caniniform; upper canines dagger-like and bilaterally compressed with weak lingual cingulum, slightly stronger posterior cingulum and no labial cingulum; P2 single-rooted, pointed, simple; P3-4 triple-rooted, non-molariform; upper molars dilambdodont with parastylar hook, tall and acute cusps, sharply defined ectoloph crests, continuous labial cingulum (ectoflexus does not extend to cingulum), and no mesostyles; M1-2 paracone and metacone of equal height; M3 labial margin angled lingually but with both paracone and metacone present; lower incisors small and biscuspid; lower premolars with primitive 13
14 size pattern of p4>p2>p3; p4 non-molariform; lower molars with strong labial cingulids and tall and acute cusps. Extant small mammals with tribosphenic dentitions and dilambdodont upper molars are almost exclusively insectivorous 42 suggesting that Onychonycteris was insectivorous like other known Eocene bats
15 Supplementary Figure 2. Basicranium of Onychonycteris finneyi (ROM 55351A, Holotype). Lettering corresponds to: a) promontorial process; b) ectotympanic; c) stylohyal (smaller arrow indicates rounded but unexpanded cranial tip); d) small orbicular apophysis of malleus. Note also that the cochlea is relatively small (see Fig. 2) and cryptocochlear. 15
16 Supplementary Figure 3. Close-up view of foot and calcar of Onychonycteris finneyi (ROM 55351A, holotype). Note that the surface texture of the calcar along its entire length is irregular and porous, unlike the smooth surfaces of the bones of the rest of the 16
17 skeleton. This texture suggests that the calcar was cartilaginous rather than calcified in Onychonycteris. Many extant bat families (megadermatids, rhinolophids, hipposiderids, most phyllostomids, mystacinids, myzopodids, and thyropterids) are characterized by presence of uncalcified calcars 18. Lack of calcification of the calcar may explain why the paratype of Onychonycteris (Supplementary Fig. 4) does not include a fossilized calcar. This also may be the case for other Eocene bats such as Icaronycteris and Archaeonycteris where the absence of a calcar simply may be the result of poor preservation. 17
18 Supplementary Figure 4. Skeleton of Onychonycteris finneyi (ROM 55055, paratype) in ventral view. Morphological features include (letters correspond to labeled points on outline drawing) Vertebrae, sternum, and ribs: no fusion of vertebrae or anterior ribs to vertebrae; first rib width similar to other ribs (a); manubrium extends laterally to the level of clavicular joint; no fusion of first costal cartilage to manubrium or first rib; second rib articulates with sternum via costal cartilage at the manubrium mesosternum joint, 6 costal cartilages articulate with mesosternum posterior to this joint; ribs lack anterior or posterior laminae (b); anterior face of manubrium small and poorly defined; length of the manubrium posterior to lateral processes is less than twice transverse width; mesosternum narrow, mean width less than half the distance between the clavicles at sternoclavicular joint; xiphisternum lacks median keel. Scapula and clavicles: infraspinous fossa of scapula relatively narrow and divided into two facets (c); lateral facet does not extend into infraglenoid region; thick lip present along axillary border of 18
19 scapula (d) ; anteromedial edge of scapula lacks projections or flanges; coracoid process stout and curves ventrolaterally; clavicle not in contact with coracoid or acromion process (e). Forelimb: shaft of radius gently arched; ulna fused to radius distal to the midpoint (f); metacarpals and proximal phalanges elongate; metacarpal formula (shortest to longest) I:II:III:IV:V; second phalanx longer than first phalanx in digits II-IV; first phalanx longer than second in digits I and V; claws present on all hand digits (g). Hindlimb: shaft of femur straight (h); femoral head slightly offset, lacking a distinct neck; fibula complete and well-developed (i); phalangeal formula ; each digit terminates in well-developed claw; first phalanx of digit I longer than first phalanx of digits II-V; overall length of first digit shorter than other digits; calcar absent but known to exist as an unossified element in the holotype (ROM 55351A) of O. finneyi (see Supplementary Fig. 3). 19
20 Supplementary Figure 5. Phylogenetic tree of bats based on unconstrained parsimony analysis of morphological data. Numbers above branches are bootstrap values, below branches are Bremer values. Note that Onychonycteris occupies the basal branch within 20
21 Chiroptera. Extinct Eocene taxa (indicated with a dagger) occupy most but not all of the basal branches; Pteropodidae (= Megachiroptera) nests among these lineages, well outside the smallest clade comprising the other extant families. 21
22 Supplementary Figure 6. Phylogenetic tree of bats based on a constrained parsimony analysis (molecular backbone tree). In this analysis, relationships of fossil taxa (indicated with a dagger) were determined based on a parsimony analysis of the same morphological data employed to recover the tree presented in Supplementary Fig. 5, but 22
23 in this case relationships among extant lineages were constrained using a backbone scaffold tree of family relationships derived from molecular studies (see Online Methods). A reduced version of this tree, in which subsets of families were grouped under their currently accepted Superfamily names, is presented in Fig. 4. Numbers above branches are bootstrap values, below branches are Bremer values. Based on results of this analysis, Onychonycteris occupies the most basal branch within Chiroptera, and a series of Eocene taxa are consecutive sister taxa to an extant chiropteran crown clade. Unambiguous synapomorphies diagnosing the smallest clade including Icaronycteris + the chiropteran crown clade (and thus not seen in Onychonycteris) consist of the following features: enlarged orbicular apophysis on the malleus; stylohyal element with an expanded, paddle-like cranial tip; enlarged cochlea; ribs with posterior laminae present; claws absent on forelimb digits III, IV, and V. Ambiguous apomorphies which diagnose this clade under some but not all optimizations include: hard palate extends posteriorly into interorbital region; pars cochlearis of petrosal loosely attached to basisphenoid via ligaments and/or thin splints of bone; cochlea phanerocochlear; posteriorly directed ventral accessory processes present on centra of cervical vertebrae 2 and 3; mesosternum articulates with five or fewer costal cartilages posterior to second rib; suprascapular process present; epitrochlea broad, width greater than or equal to 40% of width of the articular facets of humerus. 23
24 Supplementary Figure 7. Basicranium vs. cochlear width in Pteropodidae, Vespertilionidae, and Eocene bats. Vespertilionids use sophisticated laryngeal echolocation to detect, track, and capture aerial prey, while pteropodids are not capable of laryngeal echolocation 9,10,23. Some Pteropodidae (e.g., Rousettus aegyptiacus, R. amplexicaudatus, R. leschenaulti, Eonycteris spelaea) may use crude forms of echolocation involving tongue clicks or wing slaps to detect major obstacles such as walls ( 9 and references cited therein), but their abilities do not approach those of bats that use laryngeal echolocation, and their cochleae are not noticeably enlarged. 24
25 Supplementary Figure 8. Basicranium vs. cochlear width in Phyllostomidae, Molossidae, Emballonuridae, Hipposideridae, Rhinolophidae, and Mormoopidae. All of these taxa use laryngeal echolocation 9,10,
26 Supplementary Figure 9. Basicranium vs. cochlear width in Megadermatidae, Nycteridae, Natalidae, Rhinopomatidae, Thyropteridae, Mystacinidae, Craseonycteridae, and Noctilionidae. All of these taxa use laryngeal echolocation 9,10,
27 Supplementary Figure 10. Distal wing form in Onychonycteris compared with other extinct and extant bats (data for extant taxa and other Eocene forms taken from ; see 10 for measurement methods). Tip Length Ratio = Length of Hand Wing/Length of Arm Wing. Tip Area Ratio = Area of Hand Wing/Area of Arm Wing. Note that Onychonycteris exhibits the lowest known values for both Tip Length and Tip Area Ratios (ROM 55351A (Holotype), Tip Length Ratio (TLR) = 0.77, Tip Area Ratio (TAR) = 0.51; ROM (paratype), TLR = 0.80, TAR = 0.53). Among extant bats, the condition seen in Onychonycteris most closely matches that of Rhinopoma, a taxon known to use an unusual gliding-fluttering flight style 10, 12, 28. Most other echolocating bats not glide, although many members of Pteropodidae do employ gliding as part of their 27
28 flight repetoire 10. Other Eocene bats include Icaronycteris, Archaeonycteris, Palaeochiropteryx, and Hassianycteris. 28
29 3. Supplementary References 40. Findley, J. S., Studder, E. H. & Wilson, D. E. Morphological properties of bat wings. J. Mamm. 53, (1972). 41. Sargis, E. J. Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J. Morphol. 253, (2002). 42. Slaughter, B. H. in About Bats, a chiropteran biology symposium (ed Slaughter, B. H. and Walton, D. W.) (Southern Methodist Univ. Press, Dallas, 1970). 29
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