Phylogeny and systematics of early Paleogene bats

Abstract

Bats appear in the fossil record on multiple continents during the early Eocene. More than seventy Eocene bat species have been named to date, including stem bats, probable members of crown families, and others of uncertain affinity. Most phylogenetic analyses of Eocene bat relationships have focused on the handful of taxa known from nearly complete skeletal material, whereas the taxonomic relationships of more incomplete fossils have been based largely on phenetic similarities. Here we evaluate the evolutionary relationships of over 60 species of Eocene bats—including many taxa known only from fragmentary craniodental remains—in an explicitly phylogenetic context. Our analysis is based on nearly 700 morphological characters scored in 82 taxa, including 20 extant species representing all living bat families other than Pteropodidae. We found that phylogenetic relationships of Eocene bats are more complex than previously thought. Numerous families (e.g., †Archaeonycteridae, †Mixopterygidae, †Palaeochiropterygidae) and genera (e.g., †Archaeonycteris, †Icaronycteris, †Carcinipteryx) were found to be non-monophyletic as previously recognized, requiring adjustments to chiropteran taxonomy. Four major clades of stem bats were recovered in our analyses. †Microchiropteryx folieae (~ 54 Ma, India) was recovered as the earliest crown bat, occurring as the most basal lineage of Vespertilionoidea, whereas many putative crown bats were recovered among stem Chiroptera. †Tachypteron franzeni was found to be a crown bat in our analyses, as in previous studies, but it was recovered unexpectedly as a stem miniopterid. The phylogenetic relationships presented here represent the most comprehensive analysis of Eocene bat relationships completed to date, substantially improving our understanding of the position of many fossil taxa within Chiroptera and providing a foundation for future analyses of bat evolution.

Appendix 1

Synapomorphies of major clades (see Online Resource 1: Table S3 for list of synapomorphies for all clades). See Fig. 6 for numbering of nodes. Additionally, note that MorphoBank characters begin with Character 1, whereas TNT characters begin with Character 0. The characters listed below are numbered following MorphoBank formatting and therefore begin with Character 1. If comparing the characters below to the TNT script (Online Resource 2P), subtract 1 from the character number.

Fig. 6

Nodes referenced in Appendix 1

Node 1 – Clade A

24:

upper canine with raised anteromedial cingulum, but no cusp

39:

more recurved upper canine

47:

P3 absent

220:

Lower molars with lingual cusps < 75% height of labial cusps

Node 7 – Necromantidae

24:

upper canine with low anteromedial accessory cusp

25:

upper canine with anteromedial groove

29:

lingual cingulum of upper canine not steeply sloped

32:

upper canine with large distal cingulum

136:

M3 with long parastyle

245:

m1 entoconid weakly developed and low

263:

m2 entoconid weakly developed and low

Node 9 – Khonsunycteris and Witwatia (?Philisidae)

166:

lower canine without posterobasal cusp

216:

myotodont lower molars

234:

m1-2 with large hypoconulid

Node 14 – Clade B

103:

M1 preparacrista shorter than postparacrista

119:

M2 with single ectoflexus between parastyle and mesostyle region

168:

lower canine without labial cingulum

263:

m2 entoconid weak and low

Node 20 – Clade C

72:

upper molar ectocingula present but weak

174:

p2 shorter than p3

181:

p3 with anterolingual cuspule

206:

p4 with short postmetacristid

396:

one to two vertebrae articulate with ilium

398:

at least some sacral or caudal vertebrae in contact ischium by suture or fusion

450:

scapula with thick lip on axillary border

460:

scapula with crest near caudal border

468:

coracoclavicular joint absent

470:

humerofemoral index greater than 150

479:

small deltoid tubercle on humerus

563:

metacarpal II shorter than metacarpal IV

584:

digit II of wing proximal and intermediate phalanges length subequal

Node 21 – Archaeonycteridae s.l.

195:

p4 without lingual cingulid

210:

p4 tribosphenic, with distinct trigonid and talonid

253:

m1 with deep hypoflexid

255:

m2-3 paraconid slightly shorter than metaconid

275:

m3 with deep hypoflexid

Node 26 – Philisidae s.s.

82:

M1-2 angle between postparacrista and premetacrista 20 degrees or less

83:

M1-2 postparacrista does not contact premetacrista, trigon open

106:

M1 postprotocrista oriented toward a point between metacone and hypocone regions

119:

M2 with single ectoflexus between parastyle and mesostyle regions

253:

m1 with deep hypoflexid

Node 27 – Clade D

72:

upper molars with strong ectocingula

Node 29 – Hassianycteridae s.s.

187:

p3 height slightly shorter than p4 height

203:

p4 without metaconid

270:

m3 labial cingulid weakly developed

Node 30 – Clade E

188:

p3-4 subequal in length

261:

m2 labial cingulid weakly developed

270:

m3 labial cingulid weakly developed

Node 33 – Onychonycteridae s.l.

224:

lower molar cristids obliqua oriented toward protoconid

276:

m3 entocristid parallel to long axis of the tooth

Node 40 – Icaronycteridae s.l.

111:

M1 hypocone shelf small

113:

M1 hypocone incipient or poorly developed

181:

p3 anterolingual cuspule present

193:

p4 paraconid large and high

246:

m1 labial cingulid strongly developed

Node 42 – Icaronycteridae s.s.

138:

M3 paraconule present

139:

M3 postmetacrista present

140:

M3 premetacrista and postparacrista lengths subequal

Node 43 – crown bats

12:

I1 separated from i1 by large gap when cheek teeth are in occlusion

22:

upper canine anteroposteriorly elongated

85:

M1-2 mesostyle formed at contact between postparacrista and premetacrista

117:

M2 parastyle short

118:

M2 parastyle straight

136:

M3 parastyle short

194:

p4 paracristid absent

220:

lower molar lingual cusps less than 75% height of labial cusps

379:

posterior spinous process of thoracic vertebrae absent

386:

transverse processes of lumbar vertebrae caudotransversely oriented

434:

xiphoid process longer than longest sternebra

459:

scapula with convex cranial margin

477:

humerus with convex posterior edge

505:

distal styloid process of humerus well developed

518:

anconeal process of ulna further cranial than coronoid process

539:

scaphoid facet for trapezium grooved

600:

total craniocaudal length of pubis between 1.0-1.5x length of acetabulum

604:

lunate surface of acetabulum inverted U-shaped

606:

ischiatic spine absent

616:

greater trochanter of femur markedly shorter than femoral head

640:

incomplete fibula

695:

proximal phalanx of digit I of pes longer than that of digit III

Node 44 – Rhinolophoidea

24:

upper canine with low anteromedial accessory cusp

35:

upper canine with tall, conspicuous posterolateral accessory cusp that is less than ½ height of main cusp

47:

P3 absent

84:

M1-2 with narrow and deep trigon

112:

M1 hypocone shelf wider than trigon basin

159:

lower incisors not procumbent

175:

p3 absent

242:

m1 metacristid present

253:

m1 hypoflexid deep

265:

m2 hypoflexid deep

362:

cervical vertebrae C4-6 with concave posterior edge of lamina

367:

cervical vertebra C7 spinous process projects dorsally

387:

anterior transverse processes of lumbar vertebrae vertically directed

547:

trapezium smaller than trapezoid

686:

foot length 33-50% tibia length

Node 49 – Megadermatidae (Megaderma + Saharaderma)

193:

p4 paraconid absent

195:

p4 with complete lingual cingulid

208:

p4 protoconid more robust, shorter, more blunt

236:

m1 shorter than m2

245:

m1 entoconid weakly developed and low

252:

m1 talonid and trigonid subequal

263:

m2 entoconid weakly developed and low

Node 50 – Yangochiroptera

140:

M3 premetacrista subequal in length or longer than postparacrista

260:

m2 protoconid slightly higher than hypoconid

304:

medial edge of premaxilla nasal process medially twisted

366:

cervical vertebra C7 spinous process absent

395:

sacroiliac articulation fused

445:

wide infraspinous fossa of scapula

534:

sesamoid element present dorsal to trapezium–metacarpal I articulation

540:

joint for scaphoid on trapezium vertical wedge-shaped

577:

second phalanx of manus digit II unossified or absent

599:

anterior edge of pubic symphysis broad U-shaped in ventral view

617:

anteroposterior depth of greater trochanter of femur greater than transverse width

621:

third trochanter of femur less than 10% maximum length of the femur

681:

calcar present

Node 51 – Vespertilionoidea s.l.

235:

entocristid of m1-2 high crest

276:

m3 entocristid parallel to long axis of tooth

Node 53 – Myzopodidae (Myzopoda + Phasmatonycteris)

176:

single rooted p3

187:

p3 height much shorter than p4 height

188:

p3 less than or equal to ½ length of p4

189:

p3 and p4 with different crown morphologies

210:

p4 without distinct cusps

222:

lower molars with strongly developed notches in paracristid and protocristid

228:

lower molar entocristids short or disrupted so talonids drain lingually

250:

m1 paraconid situated labial to a line drawn through the metaconid and entoconid

Node 55 – Vespertilionoidea s.s.

123:

M2 postmetacrista much longer than premetacrista but not 2x length

166:

lower canine without posterobuccal cusp

188:

p3-4 subequal in length

274:

m3 protoconid slightly higher than hypoconid

499:

trochlea of humerus position midline with respect to shaft axis

500:

trochlea width intermediate with respect to condyle width

Node 58 – Molossidae (Tadarida + Cuvierimops)

30:

upper canine with well-developed, complete labial cingulum

61:

P4 lingual cingular cusp well developed

98:

M1 parastyle straight

113:

M1 hypocone well developed

130:

M2 hypocone well developed

136:

M3 parastyle long

166:

lower canine posterobasal cusp weakly developed

203:

p4 with single metaconid

Node 60 – Miniopteridae s.l. (Miniopterus + Tachypteron)

80:

M1-2 protocone more sharp and more anteriorly inclined

84:

M1-2 trigon narrow and deep

104:

M1 postmetacrista length subequal to premetacrista length

168:

M1 postmetacrista length subequal to premetacrista length

216:

lower molars nyctalodont

252:

m1 talonid and trigonid subequal in width

385:

five lumbar vertebrae present

563:

metacarpal II longer than metacarpal IV

Node 62 – Cistugidae s.l. (Cistugo + Chadronycteris)

62:

P4 labial cingulum weakly developed

67:

P4 with one distal accessory cusp

109:

M1 endoloph absent

117:

M2 with long parastyle

141:

M3 metacone indistinct, incorporated into premetacrista

Node 64 – Noctilionoidea

12:

Upper and lower first incisors in contact or separated by small gap when cheek teeth in occlusion

104:

M1 postmetacrista subequal in length to premetacrista

124:

M2 postprotocrista oriented toward midpoint between metacone and hypocone regions

216:

lower molars myotodont

506:

distal styloid process of humerus medially positioned in epitrochlea

Node 69 – Emballonuroidea s.l.

38:

posterolabial surface of upper canine rounded

67:

P4 with one distal accessory cusp

100:

M1 with single, deep ectoflexus

125:

M2 endoloph present, approaches postprotocrista at angle

196:

p4 labial cingulid weakly developed

218:

lower molar talonid basins shallow

272:

m3 cristid obliqua present but does not reach trigonid

Node 73 – Emballonuroidea s.s. (Nycteris + Saccopteryx)

38:

posterolabial surface of upper canine flattened

109:

M1 endoloph present and continuous with postprotocrista

156:

i3 present

165:

lower canine with broad posterior cingulid

224:

lower molars cristid obliqua oriented toward metaconid

242:

m1 metacristid present

253:

m1 hypoflexid deep

265:

m2 hypoflexid deep

275:

m3 hypoflexid deep

279:

m3 hypoconulid absent