The evolution of powered flight in mammals required specific developmental shifts from an ancestral limb morphology to one adapted for flight. Through studies of comparative morphogenesis, investigators have quantified points and rates of divergence providing important insights into how wings evolved in mammals. Herein I compare growth, development and skeletogenesis of forelimbs between bats and the more ancestral state provided by the rat (Rattus norvegicus) and quantify growth trajectories that illustrate morphological divergence both developmentally and evolutionarily. In addition, I discuss how wing shape is controlled during morphogenesis by applying multivariate analyses of wing bones and wing membranes and discuss how flight dynamics are stabilized during flight ontogeny. Further, I discuss the development of flight in bats in relation to the ontogenetic niche and how juveniles effect populational foraging patterns. In addition, I provide a hypothetical ontogenetic landscape model that predicts how and when selection is most intense during juvenile morphogenesis and test this model with data from a population of the little brown bat, Myotis lucifugus.

1.
Adams, R.A. (1992a) Comparative growth and development of the forearm between the little brown bat (Myotis lucifugus) and the Norway rat (Rattus norvegicus). J Morphol 214: 251–260.
2.
Adams, R.A. (1992b) Stages of development and sequence of bone formation in the little brown bat, Myotis lucifugus. J Mammal 73: 160–167.
3.
Adams, R.A. (1996) Size-specific resource partitioning among juvenile little brown bats (Myotis lucifugus): is there an ontogenetic shift? Can J Zool 74: 1204–1210.
4.
Adams, R.A. (1997) Onset of juvenile volancy and foraging patterns of little brown bats, Myotis lucifugus. J Mammal 78: 239–246.
5.
Adams, R.A. (1998) Evolutionary implications of developmental and functional integration in bat wings. J Zool Lond 246: 165–174.
6.
Adams, R.A. (2000) Wing ontogeny, shifting niche dimensions, and adaptive landscapes; in Adams, R.A., S.C. Pedersen (eds): Ontogeny, Functional Ecology and Evolution of Bats. Cambridge, Cambridge University Press, pp 275–316.
7.
Adams, R.A., T.H. Kunz (in press) Techniques for the study of growth and development in the Chiroptera; in Kunz, T.H., S. Parsons (eds): Ecological and Behavioral Methods in the Study of Bats. Baltimore, Johns Hopkins University Press.
8.
Adams, R.A., S.C. Pedersen (1994) Wings on their fingers. Nat Hist 103: 48–55.
9.
Alberch, P. (1985) Problems with the interpretation of developmental sequences. Syst Zool 34: 46–58.
10.
Amundsen. P.A., T. Bøhn, O.A. Popova, F.J. Staldvik, Y.S. Reshetnikov, N.A. Kashulin, A.A. Lukin (2003) Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild. Hydrobiologia 497: 109–1991.
11.
Bell, G. (1975) The diet and dentition of smooth newt larvae (Triturus vulgaris). J Zool Lond 176: 411–424.
12.
Buchler, E.R. (1980) The development of flight, foraging and echolocation in the little brown bat (Myotis lucifugus). Behav Ecol Sociol 6: 2111–218.
13.
Chapman, R.R. (1969) The Insects: Structure and Function. New York, Elsevier.
14.
Claessen, D., U. Dieckmann (2002) Ontogenetic niche-shifts and evolutionary branching in size-structured populations. Evol Ecol Res 4: 189–217.
15.
Coppinger, R.P., C.K. Smith (1990) A model for understanding the evolution of mammalian behavior; in Genoways, H. (ed): Current Mammalogy. New York, Plenum Press.
16.
De Fanis, E., G. Jones (1995) Post-natal growth, mother infant interactions and development of vocalizations in the vespertilionid bat Plecotus auritus. J Zool Lond 68: 411–422.
17.
Dial, K.P., R.J. Randall, T.R. Dial (2006) What use is half a wing in the ecology and evolution of birds. Bioscience 56: 437–445.
18.
Dopman, E.B., G.A. Sword, D.M. Hillis (2002) The importance of the ontogenetic niche in resource-associated divergence: evidence from generalist grasshoppers. Evolution 56: 731–740.
19.
Ellstrand, N.C. (1983) Why are juveniles smaller than their parents? Evol 37: 1091–1094.
20.
Fox, H. (1984) Amphibian Morphogenesis. Clifton, Humana Press.
21.
Goodwin, B. (1996) How the Leopard Changed Its Spots. New York, Simon & Schuster.
22.
Hill, J.E., J.D. Smith (1984) Bats: A Natural History. Austin, University of Texas Press.
23.
Hoying, K.K., T.H. Kunz (1998) Variation in size at birth and post-natal growth in the insectivorous bat Pipistrellus subflavus (Chiroptera: Vespertilionidae). J Zool Lond 245: 15–27.
24.
Hughes, P.M., R.D. Ransome, G. Jones (1995) Aerodynamic constraints on the flight ontogeny in free-living greater horseshoe bats, Rhinolophus ferrumequinum; in Hańak, V., J. Hoŕacek, J. Gaisler (eds): European Bat Research. Prague, Charles University Press.
25.
Humphrey, S.R., J.B. Cope (1976) Population ecology of the little brown bat, Myotis lucifugus, in Indiana and north-central Kentucky. Spec Publ Am Soc Mammal 4: 1–80.
26.
Jablonka, E., M.J. Lamb (1998) Bridges between development and evolution. Biol Philos 13: 119–124.
27.
Joller, V.H. (1977) Zur Ontogenese von Myotis myotis Borkhausen (verglichen mit jener von Acomys cahirinus dimidiatus). Naturforsch Ges Basel 86: 87–151.
28.
Jones, C. (1967) Growth, development and wing loading in the evening bat, Nycticeius humeralis (Rafinesque). J Mammal 48: 1–19.
29.
Jones, M., A. Laurila, N. Peuhkuri, J. Piironen, T. Seppä (2003). Timing an ontogenetic niche shift: responses of emerging salmon alevins to chemical cues from predators and competitors. Oikos 102: 155–163.
30.
Kratky, J. (1981) Postnatale Entwicklung der Wasserfledermaus, Myotis daubentoni Kuhl, und bisherige Kenntnis dieser Problematik im Rahmen der Unterordnung Microchiroptera (Mammalia: Chiroptera). Fol Mus Ref Natur Bohem Pizen Zool 16: 3–34.
31.
Kunz, T.H., E.L.P. Anthony (1982) Age estimation and postnatal growth in the bat, Myotis lucifugus. J Mammal 63: 23–32.
32.
Liem, K.F., D.B. Wake (1985) Morphology: current approaches and concepts; in Hildebrand, M., D.M. Bramble, K.F. Liem, D.B. Wake (eds): Functional Vertebrate Morphology. Cambridge, Harvard University Press, pp 336–380.
33.
Minelli, A. (2003) The Development of Animal Form: Ontogeny, Morphology, and Evolution. Cambridge, Cambridge University Press.
34.
Mohr, E. (1932) Haltung und Aufzucht des Abendseglers (Nyctalus noctula Schreb). Zool Gart Lpz 5: 106–120.
35.
Moss, M.L. (1962) The functional matrix; in Kraus, B.S., R.A. Riedel (eds): Vistas in Orthodontics. Philadelphia, Lea & Febiger, vol 35, pp 85–98.
36.
Müller, G.B. (1990) Developmental mechanisms at the origin of morphological novelty: a side effects hypothesis; in Nitecki, M.H. (ed): Evolutionary Innovations. Chicago, University of Chicago Press.
37.
Norberg, U.M. (1985) Flying, gliding and soaring; in Hildebrand, M., D.M. Bramble, K.F. Liem, D.B. Wake (eds): Vertebrate Functional Morphology. Cambridge, Harvard University Press.
38.
Oster, F.O., N. Shubin, J.D. Murray, P. Alberch (1988) Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 4: 862–884.
39.
Papadimitriou, H.M., S.M. Swartz, T.H. Kunz (1996) Ontogenetic and anatomical variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. J Zool Lond 240: 411–426.
40.
Polis, G.A. (1991) Complex interactions in deserts: an empirical critique of food-web theory. Am Nat 138: 123–155.
41.
Powers, L.V., S.C. Kandarian, T.H. Kunz (1991) Ontogeny of flight in the little brown bat, Myotis lucifugus: behavior, morphology, and muscle histochemistry. J Comp Phys A 168: 675–685.
42.
Raff, R.A. (1996) The Shape of Life: Genes Development, and the Evolution of Animal Form. Chicago, University of Chicago Press.
43.
Richardson, M.K., A.D. Chipman (2003) De- velopmental constraints in a comparative framework: a test case using variations in phalanx number during amniote evolution. J Exp Zool (Mol Dev Evol) 296B: 8–22.
44.
Rolseth, S.I., C.E. Koehler, R.M.R. Barclay (1994) Differences in the diets of juvenile and adult hoary bats, Lasiurus cinereus. J Mammal 75: 394–398.
45.
Rowe, T. (1996) Coevolution of the mammalian middle ear and neocortex. Science 273: 651–654.
46.
Sanchez-Villagra, M.R. (2002) Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. J Exp Zool (Mol Dev Evol) 294: 264–273.
47.
Sears, K.E. (2008) Molecular determinants of bat wing development. Cells Tissues Organs 187: 6–12.
48.
Sharifi, M. (2004) Postnatal growth in Myotis blythii (Chiroptera: Vespertilionidae). Mammalia 68: 283–290.
49.
Smith, K.K. (2003) Time’s arrow: heterochrony and the evolution of development. Int J Dev Biol 47: 613–621.
50.
Snodgrass, R.E. (1954) Insect metamorphosis. Smithsonian Misc Coll 122: 1–124.
51.
Speakman, J.R. (1999) The evolution of flight and echolocation: an evaluation of the energetic efficiency of reach hunting. Acta Chiroptol 1: 3–15
52.
Speakman, J.R. (2001) The evolution of flight and echolocation in bats: another leap in the dark. Mammal Rev 31: 111–130.
53.
Stern, A.A., T.H. Kunz, S.S. Bhatt (1997) Seasonal wing loading and ontogeny of flight in Phyllostomus hastatus (Chiroptera: Phyllostomidae). J Mammal 78: 1199–1209.
54.
Suthakar Isaac, S., G. Marimuthu (1997) Development of wing morphology in the Indian pygmy bat Pipistrellus mimus. J Biosci 22: 193–202.
55.
Swartz, S.M., M.S. Groves, H.D. Kim, W.R. Walsh (1996) Mechanical properties of bat wing membrane skin. J Zool Lond 239: 357–378.
56.
Swartz, S.M., K.M. Middleton (2008) Biomechanics of the bat limb skeleton: Scaling, material properties and mechanics. Cells Tissues Organs 187: 59–84.
57.
Taft, K., C.O. Handley Jr. (1991). Reproduction in a captive colony; in Handley, C.O. Jr., D.E. Wilson, A.L. Gardner (eds): Demography and Natural History of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Washington, Washington Smithsonian Press.
58.
Takimoto, G. (2003) Adaptive plasticity in ontogenetic niche shifts stabilizes consumer-resource dynamics. Am Nat 162: 93–109.
59.
Tumlison, C.R. (1990) Studies in Taxonomy and Geographic Variation in Plecotine Bats of North America; PhD dissertation, Oklahoma State University, Stillwater.
60.
van der Klaauw, C.J. (1946) Cerebral skull and facial skull. Arch Neerl Zool 7: 16–37.
61.
Wassersug, J.R., D.G. Sperry (1977) The relationship of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58: 830–839.
62.
Werner, E.E., J.F. Gilliam (1984) The ontogenetic niche and species interaction in size- structured populations. Annu Rev Ecol Syst 15: 393–425.
63.
Wilbur, H.M. (1980) Complex life cycles. Annu Rev Ecol Syst 11: 67–93.
64.
Wilson, E.O. (1985) The Biodiversity of Life. New York, Norton & Co.
65.
Wyant, K., R.A. Adams (in press) Prenatal development and skeletogenesis in the Angolan free-tailed bat (Mops condylurus). J Mammal.
66.
Yokoyama, K., T.A. Uchida (1979) Ultrastructure of postembryonic development of the pectoral muscles in the Japanese lesser horseshoe bat, Rhinolophus cornutus cornutus from the standpoint of adaptation for flight. J Fac Agric Kyushu Univ 24: 49–63.
67.
Yokoyama, K., T.A. Uchida (2005) Growth of external characters, allometry in the forelimb, and changes in the aspect ratio during the prenatal period of the Japanese lesser horseshoe bat, Rhinolophus cornutus cornutus. Ann Speleol Res Inst Japan 23: 41–59.
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