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Time’s Arrow in the Evolutionary Development of Bat Flight

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Abstract

Conceptualizing the evolution of flight in mammals is confounded by a lack of empirical evidence. In this chapter, we quantify functional ontogeny to model the evolution of flight in bats to fill in transitional gaps between a hypothetical nonvolant ancestor and volant descendents. Our data thus far indicate that bats evolved flapping flight mechanics directly with no gliding intermediate forms and that bats most likely evolved from a terrestrial, rather than arboreal, ancestor. We predict that future analysis of locomotor ontogeny in contemporary bats will be instrumental in bridging the significant gaps and discontinuities between fossil, molecular, and mechanical evidence thus far used to interpret flight evolution in mammals.

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References

  • Adams RA (1998) Evolutionary implications of developmental and functional integration in bat wings. J Zool Lond 246:165–174

    Article  Google Scholar 

  • Adams RA (2000) Wing ontogeny, shifting niche dimensions, and adaptive landscapes. In: Adams RA, Pedersen SC (eds) Ontogeny, functional ecology and evolution of bats. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Adams RA (2008) Morphogenesis in bat wings: linking development, evolution and ecology. Cells Tissues Organs 187:13–23

    Article  PubMed  Google Scholar 

  • Adams RA, Pedersen SC (2000) Ontogeny, functional ecology and evolution of bats. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Adams RA, Snode ER, Shaw JB (2012) Flapping tail membrane in bats produces potentially important thrust during horizontal takeoffs and very slow flight. PLoS ONE 10.1371/journal.pone.0047502

    Google Scholar 

  • Albertson RC, Kocher TD (2006) Genetic and developmental basis of cichlid trophic diversity. Heredity 97:211–221

    Article  PubMed  CAS  Google Scholar 

  • Allen GM (1939) Bats. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Baguñà J, Garcia-Fernández J (2003) Evo-devo: the long and winding road. Int J Dev Biol 47:705–713

    PubMed  Google Scholar 

  • Barclay RMR, Harder LD (2003) Life histories of bats: life in the slow lane. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago

    Google Scholar 

  • Bekoff A, Lau B (1980) Interlimb coordination in 20-day-old rat fetuses. J Exp Zool 214:173–175

    Article  PubMed  CAS  Google Scholar 

  • Bertossa RC (2011) Morphology and behaviour: functional links in development and evolution. Philos Trans R Soc B 366:2056–2068

    Article  Google Scholar 

  • Bishop KL (2008) The evolution of flight in bats: narrowing the field of plausible hypotheses. Q Rev Biol 83:153–169

    Article  PubMed  Google Scholar 

  • Blumberg MS (1992) Rodent ultrasonic short calls: locomotion, biomechanics and communication. J Comp Psychol 106:360–365

    Article  PubMed  CAS  Google Scholar 

  • Brakefield PM (2006) Evo-devo and constraints on selection. Trends Ecol Evol 21:362–368

    Article  PubMed  Google Scholar 

  • Brakefield PM (2011) Evo-devo and accounting for Darwin’s endless forms. Phil Trans R Soc B 366:2069–2075

    Article  PubMed  Google Scholar 

  • Breuker CJ, Debat V, Klingenberg CP (2006) Functional evo-devo. Trends Ecol Evol 21:488–492

    Article  PubMed  Google Scholar 

  • Brown RHJ (1953) The flight of birds: wing function in relation to flight speed. J Exp Biol 30:90–103

    Google Scholar 

  • Brook MH, Kaiser KK (1970) Three myosin adenosine triphosphatase’ systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18:670–672

    Article  Google Scholar 

  • Bush GL, Case SM, Wilson AC, Patton JL (1977) Rapid speciation and chromosomal evolution in mammals. Proc Natl Acad Sci 74:3942–3946

    Article  PubMed  CAS  Google Scholar 

  • Caple G, Balda RP, Willis WR (1983) The physics of leaping of leaping animals and the evolution of preflight. Am Nat 121:455–467

    Article  Google Scholar 

  • Carroll S (2010) From eternity to here: the quest for the ultimate theory of time. Oneworld, Oxford

    Google Scholar 

  • Cretekos CJ, Weatherbee SD, Chen CH, Badwaik NK, Niswander L, Behringer RR, Rasweiler JJ IV (2005) Embryonic staging systems for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancy in captive-bred animals. Dev Dyn 233:721–738

    Article  PubMed  Google Scholar 

  • Cretekos CJ, Wang Y, Green ED, Martin JF, Rasweiler JJ, Behringer RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22:121–124

    Article  CAS  Google Scholar 

  • Darwin C (1859) On the origin of species. Mentor, New York, NY

    Google Scholar 

  • Dial KP, Greene E, Irschick DJ (2008) Allometry of behavior. Trends Ecol Evol 23:394–401

    Article  PubMed  Google Scholar 

  • Dudley R, Byrnes G, Yanoviak SP, Borrell B, Brown RM, McGuire JA (2007) Origins of flight: biomechanical novelty or necessity. Annu Rev Ecol Evol Syst 38:179–201

    Article  Google Scholar 

  • Eilam D (1997) Postnatal development of body architecture and gait in several rodent species. J Exp Biol 200:1339–1350

    PubMed  CAS  Google Scholar 

  • Eilam D, Shefer G (1997) The developmental order of bipedal locomotion in the jerboa (Jaculus orientalis): pivoting, crawling, quadrupedalism and bipedalism. Dev Psychobiol 31:137–142

    Article  PubMed  CAS  Google Scholar 

  • Eldridge N, Gould SJ (1977) Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3:115–151

    Google Scholar 

  • Ferrerezi H, Giménez EA (1996) Systematic patterns and the evolution of feeding habits in Chiroptera (Mammalia; Archonta). J Comput Biol 1:75–95

    Google Scholar 

  • Ferron J (1981) Comparative ontogeny of behaviour in four species of squirrels (Sciuridae). Z Tierpsychol 55:193–216

    Article  PubMed  CAS  Google Scholar 

  • Fischer MS, Schilling N, Schmidt M, Haarhaus D, Witte HF (2002) Basic limb kinematics of small therian mammals. J Exp Biol 205:1315–1338

    PubMed  Google Scholar 

  • Gardiner DM, Torok MA, Mullen LM, Bryant SV (1999) Evolution of vertebrate limbs: robust morphology and flexible development. Am Zool 38:659–671

    Google Scholar 

  • Garstang W (1922) The theory of recapitulation: a critical restatement of the biogenetic law. Proc Linn Soc Lond Zool 35:81–101

    Article  Google Scholar 

  • Giannini NP (2012) Toward an integrative theory on the origin of bat flight. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats. Cambridge University Press, Cambridge

    Google Scholar 

  • Giannini N, Goswami A, Sánchez-Villagra MR (2006) Development of the integumentary structures in Rousettus amplexicaudatus (Mammalia: Chiroptera: Pteropodidae) during late-embryonic and fetal stages. J Mammal 87:993–1001

    Article  Google Scholar 

  • Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635–638

    Article  PubMed  CAS  Google Scholar 

  • Grande L (1994) Studies of paleoenvironments and historical biogeography in the fossil Butte and Laney members of the Green river formation. Rocky Mt Geol 30:15–32

    Google Scholar 

  • Gunnell GF, Simmons NB (2005) Fossil evidence and the origin of bats. J Mamm Evol 12:209–246

    Article  Google Scholar 

  • Gunnell GF, Simmons NB (2012) Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Guth L, Samaha FJ (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. Exp Neurol 25:138–152

    Article  PubMed  CAS  Google Scholar 

  • Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28:365–367

    Article  PubMed  CAS  Google Scholar 

  • Hall BK, Pearson BJ, Müller GB (2003) Environment, development, and evolution. MIT Press, Cambridge

    Google Scholar 

  • Hand SJ, Weisbecker V, Beck RMD, Archer M, Godhelp H, Tennyson AJD, Worthy TH (2009) Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand’s endemic mystacinids. BMC Evol Biol 9:169. doi:10.1186/1471-2148-9-169

    Article  PubMed  Google Scholar 

  • Heers AM, Dial KP (2012) From extant to extinct: locomotor ontogeny and the evolution of flight. Trends Ecol Evol 27:296–305

    Article  PubMed  Google Scholar 

  • Hermanson JW, Altenbach JS (1981) Functional anatomy of the primary down stroke muscles in a bat, Antrozous pallidus. J Mammal 62:795–800

    Article  Google Scholar 

  • Hermanson JW, Altenbach JS (1985) Functional anatomy of the shoulder and arm of the fruit-eating bat, Artibeus jamaicensis. J Zool Lond 205:157–177

    Article  Google Scholar 

  • Hill JE, Smith JD (1984) Bats: a natural history. University of Texas Press, Austin, TX

    Google Scholar 

  • Ischer T, Ireland K (2009) Locomotion performance of green sea turtle hatchlings from the Heron Island Rookery, Great Barrier Reef. Mar Biol 156:1399–1409

    Article  Google Scholar 

  • Jablonka E, Lamb MJ (1998) Bridges between development and evolution. Biol Philos 13:119–124

    Article  Google Scholar 

  • Jackson SM (2000) Glide angle in the genus Petaurus and a review of gliding in mammals. Mamm Rev 30:9–30

    Article  Google Scholar 

  • Janečka JE, Miller W, Pringle TH, Wiens F, Zitzmann A et al (2007) Molecular and genomic data identifying the closest living relative of primates. Science 318:792–794

    Article  PubMed  CAS  Google Scholar 

  • Jepson GL (1966) Early Eocene bat from Wyoming. Science 154:1333–1339

    Article  Google Scholar 

  • Jepson GL (1970) Bat origins and evolution. In: Wimsatt WA (ed) Biology of bats. Academic, New York, NY

    Google Scholar 

  • Jones KE, Bininda-Emonds ORP, Gitteman JL (2005) Bats, clocks, and rocks; diversification patterns in Chiroptera. Evolution 59:2243–2255

    PubMed  Google Scholar 

  • Kalcounis-Rüppell MC, Metheny JD, Vonhof MJ (2006) Production of ultrasound by wild Peromyscus mice. Front Zool 3:3

    Article  Google Scholar 

  • Klingenberg CP (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79–123

    Article  PubMed  CAS  Google Scholar 

  • Kmita M, Tarchini B, Zakany J, Logan M, Tabin CJ, Duboule D (2005) Early developmental arrest of mammalian limbs lacking HoxA/HoxD gene function. Nature 435:1113–1116

    Article  PubMed  CAS  Google Scholar 

  • Kunz TH, Parsons S (2009) Ecological and behavioral methods in the study of bats. Johns Hopkins University Press, Baltimore, MD

    Google Scholar 

  • Lamers AR, German RZ (2002) Ontogenetic allometry in the locomotor skeleton of specialized half-bounding mammals. J Zool Lond 258:485–495

    Article  Google Scholar 

  • Liem KF, Wake DB (1985) Morphology: current approaches and concepts. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge

    Google Scholar 

  • Lin AQ, Jin LR, Shi LM, Sun KP, Berquist SW et al (2011) Postnatal development in Andersen’s leaf-nosed bat Hipposideros pomona: flight, wing shape, and wing bone lengths. Zoology 114:69–77

    Article  PubMed  Google Scholar 

  • Mathew WD (1917) A Paleocene bat. Bull Am Mus Nat Hist 37:569–571

    Google Scholar 

  • Maynard Smith J (1952) The importance of the nervous system in the evolution of animal fight. Evolution 6:127–129

    Article  Google Scholar 

  • McMillan ME, Heller PL, Wing SL (2006) History and causes of post-Laramide relief in the Rocky Mountain orogenic plateau. Geol Soc Am Bull 118:393–405

    Article  Google Scholar 

  • Meng J, Hu Y, Wang Y, Wang X, Li C (2006) A Mesozoic gliding mammal from northeastern China. Nature 444:889–893

    Article  PubMed  CAS  Google Scholar 

  • Moody PA (1962) Introduction to evolution, 2nd edn. Harper, New York, NY

    Google Scholar 

  • Müller GB (1990) Developmental mechanisms at the origin of morphological novelty: a side effects hypothesis. In: Nitecki MN (ed) Evolutionary innovations. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Müller GB (2007) Evo-devo: extending the evolutionary synthesis. Nat Rev 8:943–948

    Google Scholar 

  • Norberg UM (1985) Evolution of vertebrate flight: an aerodynamic model for the transition from gliding to active flight. Am Nat 126:303–327

    Article  Google Scholar 

  • Norberg UM (1987) Wing form and flight mode in bats. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge

    Google Scholar 

  • Norberg UM (1990) Vertebrate flight. Springer, Berlin

    Book  Google Scholar 

  • Norberg UM, Brooke AP, Trewhella WJ (2000) Soaring and non-soaring bats of the family Pteropodidae (flying foxes, Pteropus spp.): wing morphology and flight performance. J Exp Biol 203:651–664

    Google Scholar 

  • O’Leary MA, Bloch JI, Flynn JJ, Gaudin J, Giallombardo A (2013) The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339:662–667

    Article  PubMed  CAS  Google Scholar 

  • Oster FO, Shubin N, Murray JD, Alberch P (1988) Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 4:862–884

    Article  Google Scholar 

  • Padian K (1987) A comparative phylogenetic and functional approach to the origin of vertebrate flight. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge

    Google Scholar 

  • Powers LV, Kandarian SC, Kunz TH (1991) Ontogeny of flight in the little brown bat, Myotis lucifugus: behavior, morphology, and muscle histochemistry. J Comput Phys A 168:675–685

    Google Scholar 

  • Raff RA (2007) Written in stone: fossils, genes and evo-devo. Nat Rev 8:911–920

    CAS  Google Scholar 

  • Romer AS (1959) The vertebrate story. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Rose KD (2006) The beginning of the age of mammals. John Hopkins University Press, Baltimore, MD

    Google Scholar 

  • Scheibe JS, Robins JH (1998) Morphological and performance attributes of gliding mammals. In: Steele MA, Merritt JF, Zegers DA (eds) Ecology and evolutionary biology of tree squirrels. Special publication. Virginia Museum of Natural History, Martinsville

    Google Scholar 

  • Schilling N (2005) Ontogenetic development of locomotion in small mammals-a kinematic study. J Exp Biol 208:4013–4034

    Article  PubMed  Google Scholar 

  • Schilling N, Petrovitch A (2006) Postnatal allometry of the skeleton in Tupaia glis (Scandentia: Tupaiidae) and Galea musteloides (Rodentia: Caviidae) -a test of the three-segment limb hypothesis. Zoology 109:148–163

    Article  PubMed  Google Scholar 

  • Sears KE, Behringer RR, Rasweiler JJ IV, Niswander LA (2006) Development of bat flight: morphologic and molecular evolution of bat wing digits. Proc Natl Acad Sci USA 103:6581–6586

    Article  PubMed  CAS  Google Scholar 

  • Shaw J (2011) The evolution and development of wing form, body size and flight in large- and small-bodied fruit bats (Artibeus jamaicensis and Carollia perspicillata). Dissertation, University of Northern Colorado

    Google Scholar 

  • Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818–823

    Article  PubMed  CAS  Google Scholar 

  • Siemers BM, Schauermann G, Turni H, von Merten S (2009) Why do shrews twitter? Communication or simple echo-based orientation. Biol Lett 5:593–596

    Article  PubMed  Google Scholar 

  • Simmons NB, Seymore KL, Habersetzer J, Gunnell GF (2008) Primitive early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451:818–822

    Article  PubMed  CAS  Google Scholar 

  • Smith KK (2003) Time’s arrow: heterochrony and the evolution of development. Int J Dev Biol 47:613–621

    PubMed  Google Scholar 

  • Smith T, Habersetzer J, Simmons NB, Gunnell GF (2012) Systematics and paleogeography of early bats. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats. Cambridge University Press, Cambridge

    Google Scholar 

  • Speakman JR (1999) The evolution of flight in pre-bats: an evaluation of the energetics of reach hunting. Acta Chiropterol 1:3–15

    Google Scholar 

  • Speakman JR (2001) The evolution of flight and echolocation in bats: another leap in the dark. Mamm Rev 31:111–130

    Article  Google Scholar 

  • Storch G, Sigé B, Habersetzer J (2002) Tachypteron franzeni n. gen., n. sp. earliest emballonuridbat from the middle Eocene of Messel (Mammalia, Chiroptera). Paläont Zeit 76:189

    Article  Google Scholar 

  • Stortch G, Engesser B, Wuttke M (1996) Oldest fossil record of gliding in rodents. Nature 379:439–441

    Article  Google Scholar 

  • Swan LW (1990) The concordance of ontogeny with phylogeny. Bioscience 40:376–384

    Article  Google Scholar 

  • Swartz SM, Middleton KM (2008) Biomechanics of the bat limb skeleton: scaling, material properties and mechanics. Cells Tissues Organs 187:59–84

    Article  PubMed  Google Scholar 

  • Tarchini B, Duboule D, Kmita M (2006) Regulatory constraints in the evolution of the tetrapod limb anterior-posterior polarity. Nature 26:985–988

    Article  CAS  Google Scholar 

  • Taylor GK, Thomas LR (2002) Animal flight dynamics II. Longitudinal stability in flapping flight. J Theor Biol 214:351–370

    Article  PubMed  CAS  Google Scholar 

  • Teeling EC, Springer MS, Madsen O et al (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584

    Article  PubMed  CAS  Google Scholar 

  • Teeling EC (2009) Hear, hear: the convergent evolution of echolocation in bats. Trends Ecol Evol 24:351–354

    Article  PubMed  Google Scholar 

  • Terai Y, Morikawa N, Okada N (2002) The evolution of the prodomain of bone morphogenetic protein 4 (Bmp4) in an explosively speciated lineage of East African cichlid fishes. Mol Biol Evol 19:1628–1632

    Article  PubMed  Google Scholar 

  • Tokito M, Abe T, Suzuki K (2012) The developmental basis of bat wing muscle. Nat Commun 3:1302. doi:10.1038/ncomms2298

    Article  CAS  Google Scholar 

  • Tomasi TE (1979) Echolocation by the short-tailed shrew Blarina brevicauda. J Mammal 60:751–759

    Article  Google Scholar 

  • True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3:109–119

    Article  PubMed  CAS  Google Scholar 

  • Vaughan TA (1959) Functional morphology of three bats: Eumops, Myotis, Macrotus. Pub Mus Nat Hist Univ Kansas 12:1–153

    Google Scholar 

  • Vaughan TA (1970) Flight patterns and aerodynamics. In: Wimsatt WA (ed) Biology of bats. Academic, New York, NY

    Google Scholar 

  • Veselka N, McErlain DD, Holdsworth DR, Eger J, Chhem RX, Mason MJ, Brain KL, Faure PA, Fenton MB (2010) Reply to Simmons et al. Nature 466:10. doi:10.1038/nature08737

    Google Scholar 

  • Weatherbee SD, Behringer RR, Rasweiler JJ IV, Niswander LA (2006) Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification. Proc Natl Acad Sci USA 103:15103–15107

    Article  PubMed  CAS  Google Scholar 

  • Weis-Fogh T (1973) Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production. J Exp Biol 59:169–230

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • West-Eberhard MJ (2005) Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool 304B:610–618

    Article  Google Scholar 

  • Westerga J, Gramsbergen A (1990) The development of locomotion in the rat. Dev Brain Res 57:163–174

    Article  CAS  Google Scholar 

  • Wilf P (2000) Late Paleocene-early Eocene climate changes in southwestern Wyoming: paleobotanical analysis. Bull Geol Soc Am 112:292–307

    Article  Google Scholar 

  • Williams TL (1981) Experimental analysis of the gait and frequency of locomotion in the tortoise, with a simple mathematical description. J Physiol 310:307–320

    PubMed  CAS  Google Scholar 

  • Witte HF, Biltzinger J, Hackert R, Schilling N, Schmidt M, Reich C, Fischer MS (2002) Torque patterns of the limbs of small therian mammals during locomotion on flat ground. J Exp Biol 205:1339–1353

    PubMed  Google Scholar 

  • Young RL, Badyaev AV (2007) Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal systems. Integr Comp Biol 47:234–244

    Article  PubMed  Google Scholar 

  • Zhang G, Cowled C, Shi Z, Haung Z, Bishop-Lilly KA et al (2013) Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339:456–459

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the University of Northern Colorado for providing research laboratory space and monetary funding for these projects. We thank David M. Armstrong and Scott C. Pedersen for useful comments on an earlier draft of this chapter.

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Adams, R.A., Shaw, J.B. (2013). Time’s Arrow in the Evolutionary Development of Bat Flight. In: Adams, R., Pedersen, S. (eds) Bat Evolution, Ecology, and Conservation. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7397-8_2

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