The Divergence of Echolocation Frequency in Horseshoe Bats: Moth Hearing, Body Size or Habitat?
- 377 Downloads
- 12 Citations
Abstract
A phylogenetic approach was used to test three hypotheses regarding the evolution of diversity in the echolocation frequencies used by horseshoe bats (family Rhinolophidae, genus Rhinolophus): 1) Allotonic Frequency Hypothesis (high frequency echolocation in the Rhinolophidae resulted from coevolution with moth hearing); 2) Allometry Hypothesis (echolocation frequency is negatively scaled with body size and evolutionary changes in echolocation frequencies are correlated with changes in body size in the Rhinolophidae); and 3) Foraging Habitat Hypothesis (evolution of echolocation frequency is associated with changes in habitat type). Both discrete and continuous character sets were used for ancestral state reconstructions and for investigating patterns of evolution between frequency and body size, and frequency and habitat type. Contrary to the prediction of the Allotonic Frequency Hypothesis, echolocation frequency in the Rhinolophidae did not increase over time, which would be expected if moth hearing and bat echolocation frequency coevolved. The number of extant species that exhibit calls within moth hearing ranges was not significantly different from the number of species that echolocate outside of moth hearing range. There was also no correlation between changes in frequency and changes in habitat type as predicted by the Foraging Habitat Hypothesis. Instead, the evolution of echolocation frequency within the Rhinolophidae was correlated with changes in body size as predicted by the Allometry Hypothesis.
Keywords
Rhinolophus Echolocation Phylogeny BayesTraitsNotes
Acknowledgments
We thank Dr. Iain J. Mackie for providing us with echolocation files and forearm length data for species from South East Asia. Daniel De Lemos Ribeiro, Geeta Eick, Pieter Malan, Ernest Seamark, Corrie Schoeman, and Maryalice Walker are thanked for their assistance in the field. We thank two anonymous reviewers for their valuable comments. This research was funded by grants to DSJ from the National Research Foundation (GUN 2053611) and the University Research Committee of the University of Cape Town.
References
- Acharya L, Fenton MB (1999) Bat attacks and moth defences behavior around streetlights. Can J Zool 77:27–33CrossRefGoogle Scholar
- Aldridge HDJN, Rautenbach IL (1987) Morphology, echolocation and resource partitioning in insectivorous bats. J Anim Ecol 56:763–778CrossRefGoogle Scholar
- Barclay RMR, Brigham RM (1991) Prey detection, dietary niche breadth, and body size in bats: why are aerial insectivorous bats so small? Am Naturalist 137:693–703CrossRefGoogle Scholar
- Behrend O, Kössl M, Schuller G (1999) Binaural influences on Doppler shift compensation of the horseshoe bat Rhinolophus rouxi. J Comp Physiol A 185:529–538PubMedCrossRefGoogle Scholar
- Bell GP, Fenton MB (1984) The use of Doppler-shifted echoes as a flutter detection and clutter rejection system: the echolocation and feeding behavior of Hipposideros ruber (Chiroptera: Hipposideridae). Behav Ecol Sociobiol 15:109–114CrossRefGoogle Scholar
- Bogdanowicz W, Fenton MB, Daleszczyk K (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. J Zool Lond 247:381–393CrossRefGoogle Scholar
- Boncoraglio G, Saino N (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21:134–142CrossRefGoogle Scholar
- Borissenko AV, Kruskop SV (2003) Bats of Vietnam and Adjacent Territories: an Identification Manual. Biodiversity of Vietnam Series, MoscowGoogle Scholar
- Brewer R (1998) The Science of Ecology, 2nd edn. Saunders College Publishing, FloridaGoogle Scholar
- Chen S-F, Jones G, Rossiter SJ (2009) Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Proc R Soc Lond B 276:3901–3909CrossRefGoogle Scholar
- Csorba G, Ujhelyi P, Thomas N (2003) Horseshoe Bats of the World (Chiroptera: Rhinolophidae). Alana Books, ShropshireGoogle Scholar
- Davidsonn-Watts I, Walls S, Jones G (2006) Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bat. Biol Conserv 133:118–127CrossRefGoogle Scholar
- Eckman S, Andersen HL, Wedin M (2008) The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized Ascomycota). Syst Biol 57:141–156CrossRefGoogle Scholar
- Eick GN, Jacobs DS, Matthee CA (2005) A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Mol Biol Evol 22:1869–1886PubMedCrossRefGoogle Scholar
- Fenton MB (1982) Echolocation calls and patterns of hunting and habitat use of bats (Microchiroptera) from Chillagoe, North Queensland. Aust J Zool 30:417–425CrossRefGoogle Scholar
- Fenton MB (2001) Bats. Revised edition. Checkmark Books, New YorkGoogle Scholar
- Fenton MB, Audet D, Obrist MK, Rydell J (1995) Signal strength, timing, and self-deafening: the evolution of echolocation in bats. Paleobiology 21:229–242Google Scholar
- Fenton MB, Fullard JH (1979) The influence of moth hearing on bat echolocation strategies. J Comp Physiol A 132:77–86CrossRefGoogle Scholar
- Fenton MB, Fullard JH (1981) Moth hearing and the feeding strategies of bats. Am Sci 69:266–275Google Scholar
- Francis CM, Habersetzer J (1998) Interspecific and intraspecific variation in echolocation frequency and morphology of horseshoe bats, Rhinolophus and Hipposideros. In: Kunz TH, Racey PA (eds) Bat Biology and Conservation. Smithsonian Institution Press, Washington, DC, pp 169–179Google Scholar
- Fullard JH (1982) Echolocating assemblages and the effects on moth auditory systems. Can J Zool 60:2572–2576CrossRefGoogle Scholar
- Fullard JH (1987) Sensory ecology and neuroethology of bats and moths: interactions on a global perspective. In: Fenton MB, Racey P, Rayner JMV (eds) Recent Advances in the Study of Bats. Cambridge University Press, Cambridge, pp 244–272Google Scholar
- Fullard JH (1988) The tuning of moth ears. Experientia 44:423–428CrossRefGoogle Scholar
- Fullard JH (1990) The sensory ecology of moths and bats: global lessons in staying alive. In: Evans DL, Schmidt JO (eds) Insect Defences: Adaptive Mechanisms and Strategies of Prey and Predators. State University of New York Press, Albany, pp 203–226Google Scholar
- Fullard JH (2001) Auditory sensitivity of Hawaiian moths (Lepidoptera: Noctuidae) and selective predation by the Hawaiian hoary bat (Chiroptera: Lasiurus cinereus semotus). Proc R Soc Lond B 268:1375–1380CrossRefGoogle Scholar
- Fullard JH, Jackson ME, Jacobs DS, Pavey CR, Burwell CJ (2008) Surviving cave bats: auditory and behavioral defences in the Australian noctuid moth, Speiredonia spectans. J Exp Biol 211:3808–3815PubMedCrossRefGoogle Scholar
- Fullard JH, Thomas DW (1981) Detection of certain African, insectivorous bats by sympatric tympanate moths. J Comp Physiol A 143:363–368CrossRefGoogle Scholar
- Gerhardt HC (1994) The evolution of vocalization in frogs and toads. Annu Rev Ecol Syst 25:293–324CrossRefGoogle Scholar
- Grimaldi D, Engel MS (2005) Evolution of the Insects. Cambridge University Press, CambridgeGoogle Scholar
- Guillén-Servent A, Francis CM (2006) A new species of bat of the Hipposideros bicolor group (Chiroptera: Hipposideridae) from central Laos, with evidence of convergent evolution with Sundaic taxa. Acta Chiropt 8:39–61CrossRefGoogle Scholar
- Hansen P (1979) Vocal learning: its role in adapting sound structures to long-distance propagation and a hypothesis on its evolution. Anim Behav 27:1270–1271CrossRefGoogle Scholar
- Hardy CR (2006) Reconstructing ancestral ecologies: challenges and possible solutions. Divers Distrib 12:7–19CrossRefGoogle Scholar
- Heller KG, von Helversen O (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80:178–186Google Scholar
- Hibbett DS (2004) Trends in morphological evolution in Homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches. Syst Biol 53:889–903PubMedCrossRefGoogle Scholar
- Hoagland M, Dodson B, Hauk J (2001) Exploring the Way Life Works: The Science of Biology. Jones and Bartlett Publishers, Inc., SudburyGoogle Scholar
- Jacobs DS, Barclay RMR, Walker MH (2007) The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia 152:583–594PubMedCrossRefGoogle Scholar
- Jacobs DS, Ratcliffe J, Fullard JH (2008) Beware of bats, beware of birds: the auditory responses of eared moths to bat and bird predation. Behav Ecol 19:1333–1342CrossRefGoogle Scholar
- Jiang T, Feng J, Sun K, Wang J (2008) Coexistence of two sympatric and morphologically similar bat species Rhinolophus affinis and Rhinolophus pearsoni. Prog Nat Sci 18:523–532CrossRefGoogle Scholar
- Jones G (1992) Bats vs moths: studies on the diets of rhinolophid and hipposiderid bats support the allotonic frequency hypothesis. In: Hora’beck I, Vohralik V (eds) Prague Studies in Mammalogy. Charles University Press, Prague, pp 87–92Google Scholar
- Jones G (1996) Does echolocation constrain the evolution of body size in bats? Symp Zool Soc Lond 69:111–128Google Scholar
- Jones G (1999) Scaling of echolocation call parameters in bats. J Exp Biol 202:3359–3367PubMedGoogle Scholar
- Jones G, Baker CJ (2007) Adaptive and evolutionary aspects of call design in echolocating bats. Proc Inst Acoust 29:85–99Google Scholar
- Jones G, Barlow KE (2004) Cryptic species of echolocating bats. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in Bats and Dolphins. The University of Chicago Press, Chicago, pp 345–349Google Scholar
- Jones G, Holderied MW (2007) Bat echolocation calls: adaptation and convergent evolution. Proc R Soc Lond B 274:905–912CrossRefGoogle Scholar
- Jones G, Rayner JMV (1991) Foraging behavior and echolocation of wild horseshoe bats Rhinolophus ferrumequinum and R. hipposideros (Chiroptera, Rhinolophidae). Behav Ecol Sociobiol 25:183–191CrossRefGoogle Scholar
- Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21:149–156PubMedCrossRefGoogle Scholar
- Kingston T, Jones G, Zubaid A, Kunz TH (2000) Resource partitioning in rhinolophid bats revisited. Oecologica 124:332–342CrossRefGoogle Scholar
- Kingston T, Rossiter SJ (2004) Harmonic-hopping in Wallacea’s bats. Nature 429:654–657PubMedCrossRefGoogle Scholar
- Kirsch JAW, Lapointe F-J (1997) You aren’t (always) what you eat: evolution of nectar-feeding among Old World fruitbats (Megachiroptera: Pteropodidae). In: Givnish TJ, Sytsma KJ (eds) Molecular Evolution and Adaptive Radiation. Cambridge University Press, Cambridge, pp 313–330Google Scholar
- Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50:913–925PubMedCrossRefGoogle Scholar
- Li G, Wang J, Rossiter SJ, Jones G, Cotton JA, Zhang S (2008) The hearing gene Prestin reunites echolocating bats. Proc Natl Acad Sci USA 105:13959–13964PubMedCrossRefGoogle Scholar
- Li G, Wang J, Rossiter SJ, Jones G, Zhang S (2007) Accelerated FoxP2 evolution in echolocating bats. PLoS ONE 2:e900PubMedCrossRefGoogle Scholar
- Liang Z (1993) Part of Chiroptera. In: Lao R (ed) The Mammalian Fauna of Guizhou. Guizhou Science and Technology Publishing House, Guiyang, pp 92–94Google Scholar
- Lim BK, Dunlop JM (2008) Evolutionary patterns of morphology and behavior as inferred from a molecular phylogeny of New World emballonurid bats (Tribe Diclidurini). J Mammal Evol 15:79–121CrossRefGoogle Scholar
- Maddison WP, Maddison DR (2005) Ancestral State Reconstruction package. Implimented in Mesquite. Available at http://www.mesquiteproject.org
- Maddison WP, Maddison DR (2008) Mesquite: A modular system for evolutionary analysis. Version 2.5. http://mesquiteproject.org
- Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. BioScience 51:570–581CrossRefGoogle Scholar
- Morton ES (1975) Ecological sources of selection on avian sounds. Am Naturalist 109:17–34CrossRefGoogle Scholar
- Moss CF, Sinha SR (2003) Neurobiology of echolocation in bats. Curr Opin Neurobiol 13:1–8CrossRefGoogle Scholar
- Müller R, Schnitzler H-U (1999) Acoustic flow perception in cf-bats: properties of the available cues. J Acoust Soc Am 105:2958–2966PubMedCrossRefGoogle Scholar
- Neuweiler G (1989) Foraging ecology and audition in echolocating bats. Trends Ecol Evol 4:160–166PubMedCrossRefGoogle Scholar
- Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Phil Trans R Soc Lond B 316:335–427CrossRefGoogle Scholar
- Novick A (1977) Acoustic orientation. In: Wimsatt WA (ed) Biology of Bats, Volume III. Academic Press, New York, pp 74–289Google Scholar
- Outlaw DC, Voelker G (2006) Phylogenetic tests of hypotheses for the evolution of avain migration: a case study using the Motacillidae. Auk 123:455–466CrossRefGoogle Scholar
- Pagel M (1994) Detecting correlated evolution o phylogenies: a general method for the comparative analysis of discrete characters. Proc R Soc Lond B 255:37–45CrossRefGoogle Scholar
- Pagel M (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol 48:612–622CrossRefGoogle Scholar
- Pagel M, Meade A (2004) BayesTraits package and program manual. Downloadable from www.evolution.rdg.ac.uk
- Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by Reversible-Jump Markov Chain Monte Carlo. Am Naturalist 167:808–825CrossRefGoogle Scholar
- Pfenninger M, Hrabáková M, Steinke D, Dèpraz A (2005) Why do snails have hairs? A Bayesian inference of character evolution. BMC Evol Biol 5:59. doi: 10.1186/1471-2148-5-59 PubMedCrossRefGoogle Scholar
- Pottie SA, Lane DJW, Kingston T, Lee BPY-H (2005) The microchiropteran bat fauna of Singapore. Acta Chiropt 7:237–247CrossRefGoogle Scholar
- Pye JD (1979) Why ultrasound? Endeavour 3:57–62CrossRefGoogle Scholar
- Pye JD, Roberts LH (1970) Ear movements in a hipposiderid bat. Nature 225:285–286CrossRefGoogle Scholar
- Robinson MF (1996) A relationship between echolocation calls and noseleaf widths in bats of the genera Rhinolophus and Hipposideros. J Zool Lond 239:389–393CrossRefGoogle Scholar
- Roeder KD (1967) Nerve Cells and Insect Behavior. Harvard University Press, CambridgeGoogle Scholar
- Ron SR (2008) The evolution of female mate choice for complex calls in túngara frogs. Anim Behav 76:1783–1794CrossRefGoogle Scholar
- Russo D, Mucedda M, Bello M, Biscardi S, Pidinchedda E, Jones G (2007) Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? J Biogeogr 34:2129–2138CrossRefGoogle Scholar
- Ryan MJ, Brenowitz EA (1985) The role of body size, phylogeny and ambient noise in the evolution of bird song. Am Nat 126:87–100CrossRefGoogle Scholar
- Rydell J (1992) Exploitation of insects around streetlamps in Sweden. Funct Ecol 9:744–750CrossRefGoogle Scholar
- Rydell J, Jones G, Waters D (1995) Echolocating bats and hearing moths: who are the winners? Oikos 73:419–424CrossRefGoogle Scholar
- Rydell J, Roininen H, Philip KW (2000) Persistence of bat defence reactions in high Arctic moths (Lepidoptera). Proc R Soc Lond B 267:553–557CrossRefGoogle Scholar
- Sales GD, Pye JD (1974) Ultrasonic Communication by Animals. Chapman and Hall, LondonGoogle Scholar
- Salsamendi E, Aihartza J, Goiti U, Almenar D, Garin I (2005) Echolocation calls and morphology in the Mehelyi’s (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning. Hystrix 16:149–158Google Scholar
- Scnitzler H-U (1968) Die Ultraschall-ortungslaute der Hufeisenfledermäuse (Chiroptera: Rhinolophidae) in verschiedenen Orientierungssituationen. Z Vergl Physiol 57:376–408CrossRefGoogle Scholar
- Schnitzler H-U (1987) Echoes of fluttering insects: information for echolocating bats. In: Fenton MB, Racey P, Rayner JMV (eds) Recent Advances in the Study of Bats. Cambridge University Press, Cambridge, pp 226–243Google Scholar
- Schnitzler H-U, Kalko EKV (1998) How echolocating bats search and find food. In: Kunz TH, Racey PA (eds) Bat Biology and Conservation. Smithsonian Institution Press, Washington, DC, pp 183–196Google Scholar
- Schnitzler H-U, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394CrossRefGoogle Scholar
- Schuller G, Pollak G (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats: evidence for an acoustic fovea. J Comp Pysiol A 132:47–54CrossRefGoogle Scholar
- Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: a Taxonomic and Geographic Reference. The Johns Hopkins University Press, Baltimore, pp 313–529Google Scholar
- Simmons NB, Geisler JH (1998) Phylogenetic relationships of Icaronycteris, Archaeonyteris, Hassianycteris and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull Am Mus Nat Hist 235:1–182Google Scholar
- Stoffberg S (2007) Molecular phylogenetics and the evolution of high-frequency echolocation in horseshoe bats (Genus Rhinolophus). PhD Thesis, University of Cape Town, South AfricaGoogle Scholar
- Stoffberg S, Jacobs DS, Mackie IJ, Matthee CA (2010) Molecular phylogenetics and historical biogeography of Rhinolophus bats. Mol Phylogenet Evol 54:1–9. doi: 10.1016/j.ympev.2009.09.021 PubMedCrossRefGoogle Scholar
- Strahan R (1983) Complete Book of Australian Mammals. Angus and Robertson Publishers, MelbourneGoogle Scholar
- Surlykke A (1988) Interaction between echolocating bats and their prey. In: Nachtigall PE, Moore PWB (eds) Animal Sonar: Processes and Performance. Plenum Press, New York, pp 551–566Google Scholar
- Swartz SM, Freeman PW, Stockwell EF (2004) Ecomorphology of bats: comparative and experimental approaches relating structural design to ecology. In: Kunz TH, Fenton MB (eds) Bat Ecology. University of Chicago Press, Chicago, pp 257–300Google Scholar
- Taniguchi I (1985) Echolocation sounds and hearing of the greater Japanese horseshoe bat (Rhinolophus ferrumequinum nippon). J Comp Physiol A 156:185–188CrossRefGoogle Scholar
- Teeling EC (2009) Hear, hear: the convergent evolution if echolocation in bats? Trends Ecol Evol 24:351–354PubMedCrossRefGoogle Scholar
- Teeling EC, Madsen O, Murphy WJ, Springer MS, O’Brien SJ (2003) Nuclear gene sequences confirm ancient link between New Zealand’s short-tailed bat and South American noctilionoid bats. Mol Phylogenet Evol 28:308–319PubMedCrossRefGoogle Scholar
- Thabah A, Rossiter SJ, Kingston T, Zhang S, Parsons S, Mya Mya K, Zubaid A, Jones G (2006) Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus s.l. (Chiroptera: Hipposideridae) from the Indo-Malayan region. Biol J Linn Soc 88:119–130CrossRefGoogle Scholar
- Tolley KA, Chase BM, Forest F (2008) Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern African chameleons. J Biogeogr 35:1402–1414CrossRefGoogle Scholar
- Xiang Q-Y, Thomas DT (2008) Tracking character evolution and biogrographic history through time in Cornaceae— Does choice of methods matter? J Syst Evol 46:349–374Google Scholar
- Zhang S, Zhao H, Feng J, Sheng L, Wang H, Wang H (2000) Relationship between echolocation frequency and body size in two species of hipposiderid bats. Chin Sci Bull 45:1587–1590CrossRefGoogle Scholar
- Zhao H, Zhang S, Zuo M, Zhou J (2003) Correlations between call frequency and ear lengths in bats belonging to the families Rhinolophidae and Hipposideridae. J Zool Lond 259:189–195CrossRefGoogle Scholar