Toward an integrative theory on the origin of bat flight

doi:10.1017/CBO9781139045599.011

10 - Toward an integrative theory on the origin of bat flight

Published online by Cambridge University Press: 05 June 2012

Norberto P. Giannini

Edited by

Gregg F. Gunnell and

Nancy B. Simmons

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Gregg F. Gunnell: Affiliation:
Duke University, North Carolina
Nancy B. Simmons: Affiliation:
American Museum of Natural History, New York

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Summary

In bats . . . we perhaps see traces of an apparatus originally constructed for gliding through the air rather than for flight.

Darwin (1859, p. 181)

Introduction

It is easy to grasp why bats are so successful: a small nocturnal mammal in possession of powered flight can explore resources in a relatively low-risk environment at spatial scales orders of magnitude larger than that of non-volant mammals of comparable size. As an example, the median home range of the 8–11 g vespertilionid Chalinolobus tuberculatus can be as large as 1500 ha (O'Donnell, 2001); this is the average area used, for instance, by a 300 kg herbivore, the Wapiti (Cervus elaphus canadensis; Calder, 1996). Acquisition of powered flight represented an immediate advantage to the bat lineage. As attested by the fossil record, bats reached nearly worldwide distribution early in their evolution. By the Early Eocene, bats suddenly appear in all the major landmasses they inhabit today (Gunnell and Simmons, 2005; Tejedor et al., 2005; Eiting and Gunnell, 2009). This suggests that powered flight may have played a key role in the fast expansion of bats, thereby contributing to their spectacular diversification.

Type: Chapter
Information: Evolutionary History of Bats
Fossils, Molecules and Morphology
, pp. 353 - 384

DOI: https://doi.org/10.1017/CBO9781139045599.011 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2012

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References

Adams, R. A. 1992 Comparative skeletogenesis of the forearm of the little brown bat ( and the Norway rat Journal of Morphology 214 251CrossRef Google Scholar PubMed

Adams, R. A. 1998 Evolutionary implications of developmental and functional integration in bat wingsJournal of Zoology (London) 246 165CrossRef Google Scholar

Adams, R. A. 2000 Wing ontogeny, shifting niche dimensions, and adaptive landscapesOntogeny, Functional Ecology and Evolution of BatsAdams, R. A.Pedersen, S. C.CambridgeCambridge University Press275CrossRef Google Scholar

Adams, R. A. 2008 Morphogenesis in bat wings: linking development, evolution and ecologyCells Tissues Organs 187 13CrossRef Google Scholar PubMed

Adams, R. A.Thibaud, , K. M. 2000 Ontogeny and evolution of the hindlimb and calcar: assessing phylogenetic trendsOntogeny, Functional Ecology and Evolution of BatsAdams, R. A.Pedersen, S. C.CambridgeCambridge University Press317CrossRef Google Scholar

Bishop, K. L. 2008 The evolution of flight in bats: narrowing the field of plausible hypothesesQuarterly Review of Biology 83 153CrossRef Google Scholar PubMed

Byrnes, G.Lim, N. T.-L.Spence, , A. J. 2008 Take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo ()Proceedings of the Royal Society of London Series, B 275 1007CrossRef Google Scholar

Calder, W. A. 1996 Size, Function, and Life HistoryNew YorkDover PublicationsGoogle Scholar

Caple, G.Balda, R. P.Willis, , W. R. 1983 The physics of leaping animals and the evolution of preflightAmerican Naturalist 121 455CrossRef Google Scholar

Cooper, K. L.Tabin, C. J. 2008 Understanding of bat wing evolution takes flightGenes and Development 22 121CrossRef Google Scholar PubMed

Cretekos, C. J.Weatherbee, S. D.Chen, C.-H. 2005 Embryonic staging system for the short-tailed fruit bat, , a model organism for the mammalian Order Chiroptera, based upon timed pregnancies in captive-bred animalsDevelopmental Dynamics 233 721CrossRef Google Scholar PubMed

Cretekos, C. J.Wang, Y.Green, , E. D. 2008 Regulatory divergence modifies limb length between mammalsGenes and Development 22 141CrossRef Google Scholar PubMed

Darwin, C. R. 1859 On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for LifeLondonJohn MurrayGoogle Scholar

Dechman, D. K. N.Kalko, E. K. V.Kerth, , G. 2004 Ecology of an exceptional roost: energetic benefits could explain why the bat roosts in active termite nestsEvolutionary Ecology Research 2004 1037Google Scholar

Dial, K. P.Jackson, B. E.Segre, , P. 2008 A fundamental avian wing-stroke provides a new perspective on the evolution of flightNature 451 985CrossRef Google Scholar PubMed

Eiting, T. P.Gunnell, , G. F. 2009 Global completeness of the bat fossil recordJournal of Mammalian Evolution 16 151CrossRef Google Scholar

Elangovan, V.Raghuram, H.Yuvana Satya Priya, E.Marimuthu, , G. 2004 Wing morphology and flight performance in Journal of Mammalogy 85 806CrossRef Google Scholar

Elangovan, V.Yuvana Satya Priya, E.Raghuram, H.Marimuthu, , G. 2007 Wing morphology and flight development in the short-nosed fruit bat Zoology 110 189CrossRef Google Scholar PubMed

Epstein, J. H.Olival, K. J.Pulliam, J. R. C. 2009 , a hunted migratory species with a multinational home-range and a need for regional managementJournal of Applied Ecology 46 991CrossRef Google Scholar

Farnum, C. E.Tinsley, M.Hermanson, , J. W. 2008 Forelimb versus hindlimb skeletal development in the big brown bat, : functional divergence is reflected in chondrocytic performance in autopodial growth platesCells Tissues Organs 187 35CrossRef Google Scholar PubMed

Farnum, C. E.Tinsley, M.Hermanson, , J. W. 2008 Postnatal bone elongation of the Manus versus Pes: analysis of the chondrocytic differentiation cascade in and Cells Tissues Organs 187 48CrossRef Google Scholar

Fenton, M.Crerar, , L. 1984 Cervical vertebrae in relation to roosting posture in bats. ofMammalogy 65 395CrossRef Google Scholar

Fenton, M. B.Audet, D.Obrist, M. K.Rydell, , J. 1995 Signal strength, timing, and self-deafening: the evolution of echolocation in batsPaleobiology 21 229CrossRef Google Scholar

Ferrarezi, H.Giménez, , E. A. 1996 Systematic patterns and the evolution of feeding habits in Chiroptera (Mammalia: Archonta)Journal of Comparative Biology 1 75Google Scholar

Garciadiego-Cázares, D.Rosales, C.Katoh, M.Chimal-Monroy, , J. 2004 Coordination of chondrocyte differentiation and joint formation by α5β1 integrin in the developing appendicular skeletonDevelopment 131 4735CrossRef Google Scholar PubMed

Giannini, N. P.Goswami, A.Sánchez-Villagra, , M. 2006 Development of integumentary structuresRousettus amplexicaudatusMammalia: ChiropteraPteropodidae993Google Scholar

Griffin, D. R. 1958 Listening in the DarkNew Haven, CTYale University PressGoogle Scholar

Gunnell, G. F.Simmons, , N. B. 2005 Fossil evidence and the origin of batsJournal of Mammalian Evolution 12 209CrossRef Google Scholar

Guo, X.Day, T. F.Jiang, X. 2004 Wnt/β-catenin signaling is sufficient and necessary for synovial joint formationGenes and Development 18 2404CrossRef Google Scholar PubMed

Habersetzer, J.Storch, , G. 1987 Klassifikation und funktionelle Flügelmorphologie paläogener Fledermäuse (Mammalia, Chiroptera)Courier Forschungsinstitut Senckenberg 91 11Google Scholar

Habersetzer, J.Richter, G.Storch, , G. 1994 Paleoecology of early middle Eocene bats from Messel, FRG. Aspects of flight, feeding and echolocationHistorical Biology 8 235CrossRef Google Scholar

Hedenström, A.Johansson, L. C.Wolf, M. 2007 Bat flight generates complex aerodynamic tracksScience 316 894CrossRef Google Scholar PubMed

Hermanson, J. W. 1998 Chiropteran muscle biology. A perspective from molecules to functionBat Biology and ConservationKunz, T. H.Racey, P. A.Washington, DCSmithsonian Institution Press127Google Scholar

Hermanson, J. W. 2000 Ontogeny of flight muscles: an evolutionary modelOntogeny, Functional Ecology and Evolution of BatsAdams, R. A.Pedersen, S.CambridgeCambridge University Press333CrossRef Google Scholar

Hockman, D.Cretekos, C. J.Mason, M. K. 2008 A second wave of expression during the development of the bat limbProceedings of the National Academy of Sciences, USA 105 16982CrossRef Google Scholar PubMed

Hockman, D.Mason, M. K.Jacobs, D. S.Illing, , N. 2009 The role of early development in mammalian limb diversification: a descriptive comparison of early limb development between the Natal long-fingered bat () and the mouse ()Developmental Dynamics 238 965CrossRef Google Scholar

Honeycutt, R. 2008 Small changes, big results: evolution of morphological discontinuity in mammalsJournal of Biology 7 9CrossRef Google Scholar PubMed

Jackson, S. M. 1999 Glide angle in the genus and a review of gliding in mammalsMammal Review 30 9CrossRef Google Scholar

Jackson, S. M.Schouten, P.Gliding MammalsMelbourneCSIRO Publishing

Jepsen, G. L. 1966 Early Eocene bat from WyomingScience 154 1333CrossRef Google Scholar PubMed

Jepsen, G. L. 1970 Bat origins and evolutionBiology of BatsWimsatt, W. A.New YorkAcademic Press1Google Scholar

Johnson-Murray, J. L. 1987 The comparative myology of the gliding membranes of and contrasted with the cutaneous myology of and (Marsupialia: Phalangeridae) and with selected gliding Rodentia (Sciuridae and Anamoluridae)Australian Journal of Zoology 35 101CrossRef Google Scholar

Jones, G.Teeling, E. C. 2006 The evolution of echolocation in batsTrends in Ecology and Evolution 21 149CrossRef Google Scholar PubMed

Kunz, T. H.Lumsden, , L. F. 2003 Ecology of cavity and foliage roosting batsBat EcologyKunz, T. H.Fenton, M. B.Chicago, ILUniversity of Chicago Press3Google Scholar

Kunz, T. H.Robson, , S. K. 1995 Postnatal growth and development in the Mexican free-tailed bat, : birth size, growth rates and age estimationJournal of Mammalogy 76 769CrossRef Google Scholar

Lancaster, W. C.Henson, Jr., O. W.Keating, , A. W. 1995 Respiratory muscle activity in relation to vocalization in flying batsJournal of Experimental Biology 198 175Google Scholar PubMed

Lindhe-Norberg, U. M.Brooke, A. P.Trewhella, , W. J. 2000 Soaring and non-soaring bats of the family pteropodidae (flying foxes, spp.): wing morphology and flight performanceJournal of Experimental Biology 203 651Google Scholar PubMed

Long, C. A.Zhang, G. P.George, T. F.Long, , C. F. 2003 Physical theory, origin of flight, and a synthesis proposed for birdsJournal of Theoretical Biology 224 9CrossRef Google Scholar

Logan, M. 2003 Finger or toe: the molecular basis of limb identityDevelopment 130 6401CrossRef Google Scholar PubMed

Lowenstein, T. K.Demicco, , R. V. 2006 Elevated Eocene atmospheric CO2 and its subsequent declineScience 313 1928CrossRef Google Scholar PubMed

McKay, G. M. 1989 Family PetauridaeFauna of Australia, Vol. 1B: MammaliaWalton, D. W.Richardson, B. J.CanberraAustralian Government Publishing Service665Google Scholar

Meng, J.Hu, Y.Wang, Y.Wang, X.Li, , C. 2006 A Mesozoic gliding mammal from northeastern ChinaNature 444 889CrossRef Google Scholar PubMed

Muijres, F. T.Johansson, L. C.Barfield, R. 2008 Leading-edge vortex improves lift in slow-flying batsScience 319 1250CrossRef Google Scholar PubMed

Neuweiler, G. 2000 The Biology of BatsOxfordOxford University PressGoogle Scholar

Norberg, U. M. 1969 An arrangement giving a stiff leading edge to the hand wing of batsJournal of Mammalogy 50 766CrossRef Google Scholar

Norberg, U. M. 1972 Functional osteology and myology of the wing of the dog-faced bat (É. Geoffroy) (Mammalia, Chiroptera)Zeitschrift fiir Morphologie und Okologie der Tiere 73 1CrossRef Google Scholar

Norberg, U. M. 1986 On the evolution of flight and wing forms in batsBat Flight/Fledermausflug, BIONA Report 5Nachtigall, W.StuttgartGustav Fischer13Google Scholar

Norberg, U. M. 1990 Vertebrate Flight: Mechanics, Physiology, Morphology, Ecology and EvolutionBerlinSpringer-VerlagCrossRef Google Scholar

Norberg, U. M. 1994 Wing design, flight performance, and habitat use in batsEcological Morphology: Integrative Organismal BiologyWainright, P. C.Reilly, M.Chicago, ILUniversity of Chicago Press205Google Scholar

Norberg, U. M. 1998 Morphological adaptations for flight in batsBat Biology and ConservationKunz, T. H.Racey, P. A.Washington, DCSmithsonian Institution Press93Google Scholar

Novacek, M. J. 1985 Evidence for echolocation in the oldest known batsNature 315 140CrossRef Google Scholar PubMed

O'Donnell, C. F. J. 2001 Home range and use of space by , a temperate rainforest bat from New ZealandJournal of Zoology (London) 253 253CrossRef Google Scholar

Papadimitriou, H. M.Swartz, S. M.Kunz, , T. H. 1996 Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican freetailed bat, Journal of Zoology 240 411CrossRef Google Scholar

Pennycuick, C. J. 1973 Wing profile shape in a fruit-bat gliding in a wind tunnel, determined by photogrammetryPeriodicum Biologorum 75 77Google Scholar

Pennycuick, C. J. 1986 Mechanical constraints on the evolution of flightThe Origin of Birds and the Evolution of FlightPadian, K.Memoirs of the California Academy of Sciences 8 83Google Scholar

Pirlot, P. 1977 Wing design and the origin of batsMajor Patterns in Vertebrate EvolutionHecht, M. K.Goody, P. C.Hecht, B. M.New YorkPlenum Press375CrossRef Google Scholar

Rayner, J. 1986 Vertebrate flapping mechanics and aerodynamics, and the evolution of flight in batsBat Flight/Fledermausflug, BIONA Report 5Nachtigall, W.StuttgartGustav Fischer27Google Scholar

Reilly, S. M.Wiley, E. O.Meinhardt, , D. J. 1997 An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomenaBiological Journal of the Linnean Society 60 119CrossRef Google Scholar

Richardson, M. K.Gobes, S. M. H.Van Leeuwen, A. C. 2009 Heterochrony in limb evolution: developmental mechanisms and natural selectionJournal of Experimental Zoology (Molecular Development and Evolution) 312B 639CrossRef Google Scholar

Riskin, D. K.Willis, D. J.Iriarte-Díaz, J. 2008 Quantifying the complexity of bat wing kinematicsJournal of Theoretical Biology 254 604CrossRef Google Scholar PubMed

Riskin, D. K.Iriarte-Díaz, J.Middleton, , K. M.Breuer, K. SSwartz, , S. M. 2010 The effect of body size on the wing movements of pteropodid bats, with insights into thrust and lift productionJournal of Experimental Biology 213 4110CrossRef Google Scholar PubMed

Roberts, D. 1974 Structure and function of the primate scapulaPrimate LocomotionJenkins, F. A.New YorkAcademic Press171Google Scholar

Schliemann, H.Schlosser-Sturm, , E. 1999 The shoulder joint of the Chiroptera – morphological features and functional significanceZoologischer Anzeiger 238 75Google Scholar

Schnitzler, H.-U.Kalko, , E. K. V. 2001 Echolocation by insect eating batsBioscience 51 557CrossRef Google Scholar

Schnitzler, H.-U.Moss, C. F.Denzinger, , A. 2003 From spatial orientation to food acquisition in echolocating batsTrends in Ecology and Evolution 18 386CrossRef Google Scholar

Scholey, K. 1986 The evolution of flight in batsBat Flight/Fledermausflug, BIONA Report 5Nachtigall, W.StuttgartGustav Fischer1Google Scholar

Scholey, K. 1986 The gliding and climbing locomotion of the giant red flying squirrel Bat Flight/Fledermausflug, BIONA Report 5Nachtigall, W.StuttgartGustav Fischer187Google Scholar

Sears, K. E. 2008 Molecular determinants of bat wing developmentCells Tissues Organs 187 6CrossRef Google Scholar PubMed

Sears, K. E.Behringer, R. R.Rasweiler, IV, J. JNiswander, , L. A. 2006 Development of bat flight: morphologic and molecular evolution of bat wing digitsProceedings of the National Academy of Sciences, USA 103 6581CrossRef Google Scholar PubMed

Sears, K. E.Behringer, R. R.Rasweiler, IV, J. JNiswander, , L. A. 2007 The evolutionary and developmental basis of parallel reduction in mammalian zeugopod elementsAmerican Naturalist 169 105CrossRef Google Scholar PubMed

Shen, Y.-Y.Liang, L.Zhu, Z.-H. 2010 Adaptive evolution of energy metabolism genes and the origin of flight in batsProceedings of the National Academy of Sciences, USA 107 8666CrossRef Google Scholar PubMed

Simmons, N. B. 1994 The case for chiropteran monophylyAmerican Museum Novitates 3103 1Google Scholar

Simmons, N. B. 1995 Bat relationships and the origin of flightEcology, Evolution, and Behaviour of Bats, Symposia of the Zoological Society of LondonRacey, P. A.Swift, S. M.New YorkOxford University Press27Google Scholar

Simmons, N. B.Geisler, , J. H. 1998 Phylogenetic relationships of , , , and to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in MicrochiropteraBulletin of the American Museum of Natural History 235 1Google Scholar

Simmons, N. B.Quinn, , T. H. 1994 Evolution of the digital tendon locking mechanism in bats and dermopterans: a phylogenetic perspectiveJournal of Mammalian Evolution 2 231CrossRef Google Scholar

Simmons, N. B.Seymour, K. L.Habersetzer, J.Gunnell, , G. F. 2008 Primitive early Eocene bat from Wyoming and the evolution of flight and echolocationNature 451 818CrossRef Google Scholar PubMed

Simmons, N. BSeymour, K. LHabersetzer, J.Gunnell, G. F. 2010 Inferring echolocation in ancient batsNature 466 E8CrossRef Google Scholar PubMed

Smith, J. D. 1977 Comments on flight and the evolution of batsMajor Patterns in Vertebrate EvolutionHecht, M. K.Goody, P. C.Hecht, B. M.New YorkPlenum Press427CrossRef Google Scholar

Speakman, J. R. 1993 The evolution of echolocation for predationMammals as Predators. Symposia of the Zoological Society of London 65Dunstone, N.Gorman, M. L.New YorkOxford University Press39Google Scholar

Speakman, J. R. 2001 The evolution of flight and echolocation in bats: another leap in the darkMammal Review 31 111CrossRef Google Scholar

Speakman, J. R.Racey, , P. A. 1991 No cost of echolocation for bats in flightNature 350 421CrossRef Google Scholar PubMed

Stafford, B. J. 1999 Taxonomy and ecological morphology of the flying lemurs (Dermoptera, Cynocephalidae)City University of New YorkGoogle Scholar

Suthers, R. A.Thomas, S. P.Suthers, , B. J. 1972 Respiration, wing-beat and ultrasonic pulse emission in an echolocating batJournal of Experimental Biology 56 37Google Scholar

Swartz, S. M. 1997 Allometric patterning in the limb skeleton of bats: implications for the mechanics and energetics of powered flightJournal of Morphology 234 2773.0.CO;2-6>CrossRef Google Scholar

Swartz, S. M. 1998 Skin and bones. Functional, architectural, and mechanical differentiation in the bat wingBat Biology and ConservationKunz, T. H.Racey, P. A.Washington, DCSmithsonian Institution Press109Google Scholar

Swartz, S. M.Middleton, , K. M. 2008 Biomechanics of the bat limb skeleton: scaling, material properties and mechanicsCell Tissues Organs 187 59CrossRef Google Scholar PubMed

Swartz, S. M.Bennett, M. B.Carrier, , D. R. 1992 Wing bone stresses in free flying bats and the evolution of skeletal design for flightNature 359 726CrossRef Google Scholar PubMed

Swartz, S. M.Groves, M. S.Kim, H. D.Walsh, , W. R. 1996 Mechanical properties of bat wing membrane skinJournal of Zoology 239 357CrossRef Google Scholar

Swartz, S. M.Bishop, K.Aguirre, , M.-F. I. 2005 Dynamic complexity of wing form in bats: implications for flight performanceFunctional and Evolutionary Ecology of BatsZubaid, A.McCracken, G. F.Kunz, T. H.OxfordOxford University Press110Google Scholar

Teeling, E. C. 2009 Hear, hear: the convergent evolution of echolocation in bats?Trends in Ecology and Evolution 24 351CrossRef Google Scholar PubMed

Teeling, E. C.Springer, M. S.Madsen, O. 2005 A molecular phylogeny for bats illuminates biogeography and the fossil recordScience 307 580CrossRef Google Scholar PubMed

Tejedor, M. F.Czaplewski, N. J.Goin, F. J.Aragón, , E. 2005 The oldest record of South American batsJournal of Vertebrate Paleontology 25 990CrossRef Google Scholar

Thewissen, J. G. M.Babcock, , S. K. 1992 Distinctive cranial and cervical innervation of wing muscles: new evidence for bat monophylyScience 251 934CrossRef Google Scholar

Thomas, A. L. R.Jones, G.Rayner, J. M. V.Hughes, , P. M. 1990 Intermittent gliding flight in the pipistrelle bat () (Chiroptera: Vespertilionidae)Journal of Experimental Biology 149 407Google Scholar

Thomas, S. P. 1987 The physiology of bat flightRecent Advances in the Study of BatsFenton, M. B.Racey, P.Rayner, R. M. V.CambridgeCambridge University Press75Google Scholar

Thorington, Jr., R. W.Heaney, L. R. 1981 Body proportions and gliding adaptations of flying squirrels (Petauristinae)Journal of Mammalogy 62 101CrossRef Google Scholar

Tokita, M. 2006 Normal embryonic development of the Japanese pipistrelle, Zoology 109 137CrossRef Google Scholar

Tschapka, M. 2008 Rudimentary finger claws in a flower-visiting phyllostomid batActa Chiropterologica 10 177CrossRef Google Scholar

Vaughan, T. A. 1959 Functional morphology of three bats: , , University of Kansas Publications, Museum of Natural History 12 1Google Scholar

Vaughan, T. A. 1970 The skeletal systemBiology of Bats 1Wimsatt, W. A.New YorkAcademic Press98Google Scholar

Veselka, N.McErlain, D. D.Holdsworth, D. W. 2010 A bony connection signals laryngeal echolocation in batsNature 463 939CrossRef Google Scholar PubMed

Watts, P.Mitchell, E. J.Swartz, , S. M. 2001 A computational model for estimating the mechanics of horizontal flapping flight in bats: model description and validationJournal of Experimental Biology 204 2873Google Scholar

Weatherbee, S. D.Behringer, R. R.Rasweiler, J. J.Niswander, , L. A. 2006 Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversificationProceedings of the National Academy of Sciences, USA 103 15103CrossRef Google Scholar PubMed

Wilf, P.Labandeira, C. C. 1999 Response of plant-insect associations to Paleocene-Eocene warmingScience 284 2153CrossRef Google Scholar PubMed

Wyant, K. A.Adams, R. A. 2007 Prenatal growth and development in the Angolan free tailed batMops condylurusChiropteraMolossidae 88Google Scholar

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