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1 - Phylogenies, fossils and functional genes: the evolution of echolocation in bats

Published online by Cambridge University Press:  05 June 2012

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

Introduction

Bats are one of the most successful orders of mammals on this planet. They account for over 20% of living mammalian diversity (~ 1200 species), and are distributed throughout the globe, absent only from the extreme latitudes (Simmons, 2005). Bats are the only living mammals that are capable of true self-powered flight, and likewise they are the only mammals capable of sophisticated laryngeal echolocation (Macdonald, 2006). Their global success is largely attributed to these novel adaptations (Jones and Teeling, 2006). Echolocation occurs when a bat emits a brief laryngeal-generated sound that can vary in duration (0.3–300 ms) and in frequency (8–210 kHz) and interprets the returning echoes to perceive its environment (Fenton and Bell, 1981; Thomas et al., 2004). Calls and echoes can be separated either in time or in frequency (Jones, 2005). Some bats (e.g., horseshoe bats, leaf-nosed bats and mustached bats) emit long constant-frequency calls with Doppler shift compensation (CF/DSC) by taking the velocity of their flight into account and adjusting the frequency of their outgoing calls to ensure that the incoming echoes return at a specific frequency (Thomas et al., 2004; Jones, 2005). Most other bats emit low-duty-cycle frequency-modulated calls, and separate outgoing calls and incoming echoes temporally (Thomas et al., 2004; Jones, 2005).

Echolocation calls show a great diversity in shape, duration and amplitude, and are correlated with the parameters of a bat's environment (Jones and Teeling, 2006; Jones and Holderied, 2007). The auditory capabilities of bats are extraordinary. Bats produce and interpret some of the “loudest” naturally produced airborne sounds ever recorded (130 dB; Jones, 2005), and are also capable of hearing some of the “quietest” sounds of any mammal (~-20 dB; Neuweiler, 1990). Despite the magnitude and functionality of this spectacular form of sensory perception, the evolutionary history of echolocation is still controversial. This has stemmed from inconsistent and unresolved phylogenies (Simmons and Geisler, 1998; Van Den Bussche and Hoofer, 2004; Eick et al., 2005; Teeling et al., 2005), and an incomplete (Teeling et al., 2005; Eiting and Gunnell, 2009) and differentially interpreted fossil record (Simmons et al., 2008; Veselka et al., 2010) that allows for alternate interpretations of gain and loss of auditory function, and lack of molecular echolocation signatures (Teeling, 2009).

Type
Chapter
Information
Evolutionary History of Bats
Fossils, Molecules and Morphology
, pp. 1 - 22
Publisher: Cambridge University Press
Print publication year: 2012

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References

Ao, L.Mao, X.Nie, W. 2007 Karyotypic evolution and phylogenetic relationships in the order Chiroptera as revealed by G-banding comparison and chromosome paintingChromosome Research 15 257Google ScholarPubMed
Baker, R. J.Longmire, J. L.Maltbie, M.Hamilton, M. J.Van Den Bussche, R. A. 1997 DNA synapomorphies for a variety of taxonomic levels from a cosmid library from the New World batMacrotus waterhousii. Systematic Biology 46 579CrossRefGoogle ScholarPubMed
Baker, R. J.Hoofer, S. R.Porter, C. A.Van Den Bussche, R. A. 2003 Diversification among New World Leaf-Nosed Bats: an evolutionary hypothesis and classification inferred from digenomic congruence of DNA sequenceOccasional Papers, Museum of Texas Tech University 230 1Google Scholar
Eick, G. N.Jacobs, D. S.Matthee, C. A. 2005 A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera)Molecular Biology and Evolution 22 1869CrossRefGoogle Scholar
Eiting, T. P.Gunnell, G. F. 2009 Global completeness of the bat fossil recordJournal of Mammalian Evolution 16 151CrossRefGoogle Scholar
Fenton, M. B.Bell, G. P. 1981 Recognition of species of insectivorous bats by their echolocation callsJournal of Mammalogy 62 233CrossRefGoogle Scholar
Genome 10K Community of Scientists 2009 Genome10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate speciesJournal of Heredity 100 659CrossRefGoogle Scholar
Gunnell, G. F.Simmons, N. B. 2005 Fossil evidence and the origin of batsJournal of Mammalian Evolution 12 209CrossRefGoogle Scholar
Gunnell, G. F.Jacobs, B. F.Herendeen, P. S. 2003 Oldest placental mammal from sub-Saharan Africa: Eocene microbat from Tanzania – evidence for early evolution of sophisticated echolocationPalaeontologia Electronica 5 10Google Scholar
Hayden, S.Bekaert, M.Crider, T. A. 2010 Ecological adaptation determines functional mammalian olfactory subgenomesGenome Research 20 1CrossRefGoogle ScholarPubMed
Higgins, D. G.Sharp, P. M. 1988 CLUSTAL: a package for performing multiple sequence alignment on a microcomputerGene 73 237CrossRefGoogle ScholarPubMed
Hilgert, N.Smith, R. J. H.Van Camp, G. 2009 Forty-six genes causing nonsyndromic hearing impairment: which ones should be analyzed in DNA diagnostics?Mutation Research/Reviews in Mutation Research 681 189CrossRefGoogle ScholarPubMed
Hollar, L. J.Springer, M. S. 1997 Old World fruitbat phylogeny: evidence for convergent evolution and an endemic African cladeProceedings of the National Academy of Sciences, USA 94 5716CrossRefGoogle ScholarPubMed
Hoofer, S. RVan Den Bussche, R. A. 2003 Molecular phylognetics of the chiropteran family VespertilionidaeActa Chiropterologica 5 1CrossRefGoogle Scholar
Hutcheon, J. M.Kirsch, J. A. W. 2004 Camping in a different tree: results of molecular systematic studies of bats using DNA-DNA-hybridizationJournal of Mammalian Evolution 11 17CrossRefGoogle Scholar
Hutcheon, J. M.Kirsch, J. A. W. 2006 A moveable face: deconstructing the Microchiroptera and a new classification of extant batsActa Chiropterologica 8 1CrossRefGoogle Scholar
Hutcheon, J. M.Kirsch, J. A. W.Pettigrew, J. D. 1998 Base compositional biases and the bat problem. III. The question of microchiropteran monophylyPhilosophical Transactions of the Royal Society of London B 353 607CrossRefGoogle ScholarPubMed
Jones, G. 2005 EcholocationCurrent Biology 15 R484CrossRefGoogle ScholarPubMed
Jones, G.Holderied, M. W. 2007 Bat echolocation calls: adaptation and convergent evolutionProceedings of the Royal Society of London B 276 905CrossRefGoogle Scholar
Jones, G.Teeling, E. C. 2006 The evolution of echolocation in batsTrends in Ecology and Evolution 21 149CrossRefGoogle ScholarPubMed
Jones, K. E.Purvis, A.MacLarnon, A.Bininda-Emonds, O. R. P.Simmons, N. B. 2002 A phylogenetic supertree of the bats (Mammalia: Chiroptera)Biological Reviews 77 223CrossRefGoogle Scholar
Kirwan, J. 2010 The molecular evolution of hearing in mammalsUniversity College DublinIrelandGoogle Scholar
Koopman, K. F. 1994 Chiroptera: systematicsHandbook of ZoologyBerlin, GermanyWalter de GruyterGoogle Scholar
Lander, E. S.Linton, L. M.Birren, B. 2001 Initial sequencing and analysis of the human genomeNature 409 860CrossRefGoogle ScholarPubMed
Li, G.Wang, J.Rossiter, S. J.Jones, G.Zhang, S. 2007 Accelerated FoxP2 evolution in echolocating batsPLoS ONE 2 e900CrossRefGoogle ScholarPubMed
Li, G.Wang, J.Rossiter, S. J. 2008 The hearing gene Prestin reunites echolocating batsProceedings of the National Academy of Sciences, USA 105 13959CrossRefGoogle ScholarPubMed
Li, Y.Liu, Z.Shi, P.Zhang, J. 2010 The hearing gene Prestin unites echolocating bats and whalesCurrent Biology 20 R55CrossRefGoogle ScholarPubMed
Liu, F. R.Miyamoto, M. M. 1999 Phylogenetic assessment of molecular and morphological data for eutherian mammalsSystematic Biology 48 54CrossRefGoogle ScholarPubMed
Liu, Y.Cotton, J. A.Shen, B. 2010 Convergent sequence evolution between echolocating bats and dolphinsCurrent Biology 20 R53CrossRefGoogle ScholarPubMed
Macdonald, D. W. 2006 The Encyclopedia of MammalsOxfordOxford University PressGoogle Scholar
Miller-Butterworth, C. M.Murphy, W. J.O'Brien, S. J. 2007 A family matter: conclusive resolution of the taxonomic position of the Long-fingered Bats, Molecular Biology and Evolution 24 1553CrossRefGoogle Scholar
Neuweiler, G. 1990 Auditory adaptations for prey capture in echolocating batsPhysiological Reviews 70 615CrossRefGoogle ScholarPubMed
Novacek, M. J. 1985 Evidence for echolocation in the oldest known batsNature 315 140CrossRefGoogle ScholarPubMed
Pierson, E. D. 1986 Molecular systematics of the Microchiroptera: higher taxon relationships and biogeographyUniversity of CaliforniaBerkeleyGoogle Scholar
Porter, C. A.Goodman, M.Stanhope, M. J. 1996 Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand Factor geneMolecular Phylogenetics and Evolution 5 89CrossRefGoogle ScholarPubMed
Posada, D.Crandall, K. A. 1998 Modeltest: testing the model of DNA substitutionBioinformatics 14 817CrossRefGoogle ScholarPubMed
Rambaut, A. E. 1996 tree.bio.ed.ac.uk/software/seal/
Simmons, N. B. 1998 A reappraisal of interfamilial relationships of batsBat Biology and ConservationKunz, T. H.Racey, P. A.Washington, DCSmithsonian Institution Press3Google Scholar
Simmons, N. B. 2005 Order ChiropteraMammal Species of the World: A Taxonomic and Geographic ReferenceWilson, D. E.Reeder, D. M.Baltimore, MDJohns Hopkins University Press312Google 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.Seymour, K. L.Habersetzer, J.Gunnell, G. F. 2008 Primitive early Eocene bat from Wyoming and the evolution of flight and echolocationNature 451 818CrossRefGoogle ScholarPubMed
Simmons, N. BSeymour, K. LHabersetzer, J.Gunnell, G. F. 2010 Inferring echolocation in ancient batsNature 466 E8CrossRefGoogle ScholarPubMed
Springer, M. S.Teeling, E. C.Madsen, O.Stanhope, M. J.de Jong, W. W. 2001 Integrated fossil and molecular data reconstruct bat echolocationProceedings of the National Academy of Sciences, USA 98 6241CrossRefGoogle ScholarPubMed
Stanhope, M. J.Czelusniak, J.Si, J. S.Nickerson, J.Goodman, M. 1992 A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophylyMolecular Phylogenetics and Evolution 1 148CrossRefGoogle ScholarPubMed
Swofford, D. L. 2002 PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods)Sunderland, MASinauer AssociatesGoogle Scholar
Teeling, E. C. 2009 Hear, hear: the convergent evolution of echolocation in bats?Trends in Ecology and Evolution 24 351CrossRefGoogle ScholarPubMed
Teeling, E. C.Scally, M.Kao, D. J. 2000 Molecular evidence regarding the origin of echolocation and flight in batsNature 403 188CrossRefGoogle ScholarPubMed
Teeling, E. C.Springer, M. S.Madsen, O. 2005 A molecular phylogeny for bats illuminates biogeography and the fossil recordScience 307 580CrossRefGoogle ScholarPubMed
Thomas, J.Moss, C.Vater, M. 2004 Echolocation in Bats and DolphinsChicago, ILUniversity of Chicago PressGoogle Scholar
Van Den Bussche, R. A.Hoofer, S. R. 2004 Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxaJournal of Mammalogy 85 3212.0.CO;2>CrossRefGoogle Scholar
Venter, J. C.Adams, M. D.Myers, E. W. 2001 The sequence of the human genomeScience 291 1304CrossRefGoogle ScholarPubMed
Veselka, N.McErlain, D. D.Holdsworth, D. W. 2010 A bony connection signals laryngeal echolocation in batsNature 463 939CrossRefGoogle ScholarPubMed
Via, S. 2009 Natural selection in action during speciationProceedings of the National Academy of Sciences, USA 106 9939CrossRefGoogle ScholarPubMed
Woodburne, M. O.Gunnell, G. F.Stucky, R. K. 2009 Climate directly influences Eocene mammal faunal dynamics in North AmericaProceedings of the National Academy of Sciences, USA 106 13399CrossRefGoogle ScholarPubMed

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