Female mate choice can drive the evolution of high frequency echolocation in bats: A case study with Rhinolophus mehelyi

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Puechmaille, Sébastien J ^a,b,c,h   Borissov, Ivailo M ^a,c   Zsebok, Sándor ^a,c,d   Allegrini, Benjamin ^e   Hizem, Mohammed ^f   Kuenzel, Sven ^g   Schuchmann, Maike ^a,c   Teeling, Emma C ^b   Siemers, Björn M ^a,c  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c Tabachka Bat Research Station   (Bulgaria)

^d EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^e Naturalia Environnement Gallargues le Montueux   (France)

^f University Tunis El Manar   (Tunisia)

^g MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^h UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; AUDITORY STIMULATION; BAT; BODY HEIGHT; BODY SIZE; BODY WEIGHT; CASE STUDY; CONTROLLED STUDY; ECHOLOCATION; FEMALE; HEARING; MALE; MATE CHOICE; NONHUMAN; REPRODUCTIVE SUCCESS; RHINOLOPHUS MEHELYI; SEXUAL SELECTION; STIMULUS RESPONSE; ANIMAL; MOLECULAR GENETICS; PHYSIOLOGY; VOCALIZATION;

ANIMALS; CHIROPTERA; ECHOLOCATION; FEMALE; MALE; MATING PREFERENCE, ANIMAL; MOLECULAR SEQUENCE DATA; VOCALIZATION, ANIMAL;

EID: 84904985516     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103452     Document Type: Article

References (72)

1. Davies NB, Halliday TR (1978) Deep croaks and fighting assessment in toads Bufo bufo. Nature 274: 683-685.
2. Galeoti P, Sacchi R, Pellitteri Rosa D, Fasola M (2005) Female preference for fast-rate, high-pitched calls in Hermann's tortoises Testudo hermanni. Behavioral Ecology 16: 301-308. (Pubitemid 40112976)
3. Gray DA (1997) Female house crickets, Acheta domesticus, prefer the chirps of large males. Animal Behaviour 54: 1553-1562.
4. Riede T, Fitch WT (1999) Vocal length and acoustics of vocalization in the domestic dog (Canis familiaris). The Journal of Experimental Biology 202: 2859-2867.
5. Sell A, Bryant GA, Cosmides L, Tooby J, Sznycer D, et al. (2010) Adaptations in humans for assessing physical strength from the voice. Proceedings of the Royal Society B: Biological Sciences 277: 3509-3518. doi:10.1098/rspb.2010.0769.
6. Charlton B, Reby D, McComb K (2007) Female red deer prefer the roars of larger males. Biology Letters 3: 382-385.
7. Puts DA (2005) Mating context and menstrual phase affect women's preferences for mal voice pitch. Evolution and Human Behavior 26: 388-397.
8. Ellers J, Boggs CL (2003) Evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies. Evolution 57: 1100-1106. (Pubitemid 36726564)
9. Bonduriansky R (2011) Sexual selection and conflict as engines of ecological diversification. The American naturalist 178: 729-745. doi:10.1086/662665.
10. Fenton MB (2003) Eavesdropping on the echolocation and social calls of bats. Mammal Review 33: 193-204.
11. Fenton MB (1985) Communication in the Chiroptera. Bloomington: Indiana University Press. 161 p.
12. Jones G, Holderied MW (2007) Bat echolocation calls: adaptation and convergent evolution. Proceedings of the Royal Society of London, B 274: 905-912. (Pubitemid 47056739)
13. Schnitzler H-U, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends in Ecology and Evolution 18: 386-393.
14. Siemers BM, Schnitzler H-U (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429: 657-661. (Pubitemid 38812316)
15. Jones G, Siemers B (2011) The communicative potential of bat echolocation pulses. Journal of Comparative Physiology A 197: 447-457.
16. Jones G (1997) Acoustic signals and speciation: the roles of natural and sexual selection in the evolution of cryptic species. Advances in the Study of Behavior 26: 317-354.
17. Puechmaille SJ, Ar Gouilh M, Piyapan P, Yokubol M, Khin Mie Mie, et al. (2011) The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nature Communications 2: 573. doi:10.1038/ncomms1582.
18. Knörnschild M, Jung K, Nagy M, Metz M, Kalko E (2012) Bat echolocation calls facilitate social communication. Proceedings of the Royal Society B: Biological Sciences 279: 4827-4835. doi:10.1098/rspb.2012.1995.
19. Schuchmann M, Puechmaille SJ, Siemers BM (2012) Horseshoe bats recognise the sex of conspecifics from their echolocation calls. Acta Chiropterologica 14: 161-166. doi:10.3161/150811012x654376.
20. Jacobs DS, Barclay RM, Walker MH (2007) The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia 152: 583-594. (Pubitemid 46776460)
21. Canadian Council On Animal Care (2003) CCAC species-specific recommendations on: BATS. 1-9.
22. Schuchmann M, Siemers BM (2010) Variability in echolocation call intensity in a community of horseshoe bats: a role for resource partitioning or communication? PLoS ONE 5: e12842. doi:10.1371/journal.pone.0012842.
23. Siemers BM, Beedholm K, Dietz C, Dietz I, Ivanova T (2005) Is species identity, sex age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica 7: 259-274. (Pubitemid 43013965)
24. Huffman RF, Henson OW (1993) Labile cochlear tuning in the mustached bat I. Concomitant shifts in biosonar emission frequency. Journal of Comparative Physiology A 171: 725-734.
25. Huffman RF, Henson OW (1993) Labile cochlear tuning in the mustached bat II. Concomitant shifts in neural tuning. Journal of Comparative Physiology A 171: 735-748.
26. Sueur J, Aubin T, Simonis C (2008) Seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18: 213-226.
27. R Development Core Team (2013) R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
28. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891. doi:10.1111/j.1600-0706.2009.17643.x.
29. Dietz C, Dietz I, Siemers BM (2007) Growth of horseshoe bats (Chiroptera: Rhinolophidae) in temperate continental conditions and the influence of climate. Mammalian Biology 72: 129-144. (Pubitemid 46497883)
30. Siemers BM, Ivanova T (2004) Ground gleaning in horseshoe bats: comparative evidence from Rhinolophus blasii, R. euryale and R. mehelyi. Behavioral Ecology and Sociobiology 56: 464-471. (Pubitemid 39219071)
31. Schuchmann M, Siemers BM (2010) Behavioral evidence for community-wide species discrimination from echolocation calls in bats. The American Naturalist 176: 72-82. doi:10.1086/652993.
32. Ma J, Kobayasi K, Zhang S, Metzner W (2006) Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum. Journal of Comparative Physiology A 192: 535-550. doi:10.1007/s00359-006-0094-9.
33. Liu Y, Metzner W, Feng J (2013) Vocalization during copulation behavior in greater horseshoe bats, Rhinolophus ferrumequinum. Chinese Science Bulletin 58: 2179-2184. doi:10.1007/s11434-013-5793-3.
34. Puechmaille SJ, Hizem WM, Allegrini B, Abiadh A (2012) Bat fauna of Tunisia: review of records and new records, morphometrics and echolocation data. Vespertilio 16: 211-239.
35. Castoe TA, Poole AW, Gu W, Jason de Koning AP, Daza JM, et al. (2010) Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Molecular Ecology Resources 10: 341-347.
36. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press. 365-386.
37. Vallone PM, Butler JM (2004) Auto-Dimer: a screening tool for primer-dimer and hairpin structures. BioTechniques 37: 226-231. (Pubitemid 39050463)
38. Puechmaille SJ, Yokubol M, Piyapan P, Ar Gouilh M, Khin Mie Mie, et al. (2009) Characterization and multiplex genotyping of 16 polymorphic microsatellite loci in the endangered bumblebee-bat, Craseonycteris thonglongyai (Chiroptera: Craseonycteridae). Conservation Genetics 10: 1073-1076. doi:10.1007/s10592-008-9691-1.
39. Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. BioTechniques 20: 1004-1010. (Pubitemid 126509230)
40. Puechmaille SJ, Mathy G, Petit E (2005) Characterization of 14 polymorphic microsatellite loci for the lesser horseshoe bat, Rhinolophus hipposideros (Rhinolophidae, Chiroptera). Molecular Ecology Notes 5: 941-944. doi:10.1111/j.1471-8286.2005.01123.x. (Pubitemid 43278017)
41. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248-249.
42. Van Oosterhout C, Hutchison WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538. (Pubitemid 39147523)
43. Wang J (2011) Coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources 11: 141-145. doi:10.1111/j.1755-0998.2010.02885.x.
44. Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160: 1203-1215.
45. Lynch M (1988) Estimation of relatedness by DNA fingerprinting. Molecular Biology and Evolution 5: 584-599.
46. Li CC, Weeks DE, Chakravarti A (1993) Similarity of DNA fingerprints due to chance and relatedness. Human Heredity 43: 45-52. (Pubitemid 23097294)
47. Milligan BG (2003) Maximum-Likelihood estimation of relatedness. Genetics 163: 1153-1167.
48. Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genetics Research 89: 135-153. doi:10.1017/ S0016672307008798.
49. Ulanovsky N, Moss CF (2008) What the bat's voice tells the bat's brain. Proceedings of the National Academy of Sciences of the United States of America 105: 8491-8498. (Pubitemid 351987709)
50. Francis CM, Habersetzer J (1998) Interspecific and intraspecific variation in echolocation call frequency and morphology of horseshoe bats, Rhinolophus and Hipposideros. In: Kunz TH, Racey PA, editors. Bat: Biology and Conservation. Washington: Smithsonian Institution Press. 169-179.
51. Maynard Smith J (1991) Theories of sexual selection. Trends in Ecology & Evolution 6: 146-151.
52. Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. The Quarterly Review of Biology 84: 3-27.
53. Simmons LW (1988) The calling song of the field cricket, Gryllus bimaculatus (De Geer): constraints on transmission and its role in intermale competition and female choice. Animal Behaviour 36: 380-394.
54. Dietz C, Von Helversen O, Nill D (2009) Bats of Britain, Europe & Northwest Africa. London: A & C Black Publishers Ltd. 400 p.
55. Ward HL, Ransome RD, Jones G, Rossiter SJ (2014) Determinants and patterns of reproductive success in the Greater Horseshoe bat during a population recovery. PLoS ONE 9: e87199. doi:10.1371/journal.pone.0087199.
56. Jones G, Ransome RD (1993) Echolocation calls of bats are influenced by maternal effects and change over lifetime. Proceedings of the Royal Society of London, B 252: 125-128. (Pubitemid 23191545)
57. Crichton EG, Krutzsch PH, editors (2000) Reproductive biology of bats. London: Academic Press. 528 p.
58. Zahavi A (1975) Mate selection-A selection for a handicap. Journal of Theoretical Biology 53: 205-214.
59. Scherrer JA, Wilkinson GS (1993) Evening bat isolation calls provide evidence for heritable signatures. Animal Behaviour 46: 847-860.
60. Masters WM, Raver KAS, Kazial KA (1995) Sonar signals of big brown bats, Eptesicus fuscus, contain information about individual identity, age and family affiliation. Animal Behaviour 50: 1243-1260. (Pubitemid 26450407)
61. Salsamendi E, Aihartza JR, Goiti U, Almenar D, Garin I (2005) Echolocation calls and morphology in the Mehely's (Rhinolophus mehelyi) and mediterranean (R. euryale) horseshoe bats: implications for ressource partitioning. Hystrix, Italian Journal of Mammalogy 16: 149-158.
62. Russo D, Mucedda M, Bello M, Biscardi S, Pidinchedda E, et al. (2007) Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? Journal of Biogeography 34: 2129-2138. (Pubitemid 350125999)
63. Jiang T, You Y, Liu S, Lu G, Wang L, et al. (2013) Factors affecting geographic variation in echolocation calls of the endemic Myotis davidii in China. Ethology 119: 881-890. doi:10.1111/eth.12130.
64. Thong VD, Puechmaille SJ, Denzinger A, Csorba G, Dietz C, et al. (2012) A new species of Hipposideros (Chiroptera: Hipposideridae) from Vietnam. Journal of Mammalogy 93: 1-11. doi:10.1644/11-MAMM-A-073.1.
65. Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. Journal of Zoology, London 261: 21-33. (Pubitemid 37143475)
66. Wyatt TD (2014) Pheromones and animal behavior. Chemical signals and signatures. Cambridge, United Kingdom: Cambridge University Press. 419 p.
67. Voigt CC, Behr O, Caspers B, Von Helversen O, Knornschild M, et al. (2008) Songs, scents, and senses: sexual selection in the greater sac-winged bat, Saccopteryx bilineata. Journal of Mammalogy 89: 1401-1410.
68. Hayden S, Bekaert M, Crider TA, Mariani S, Murphy WJ, et al. (2010) Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Research 20: 1-9.
69. Jones G, Teeling EC, Rossiter S (2013) From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats. Frontiers in Physiology 4: 1-16. doi:10.3389/fphys.2013.00117.
70. Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends in Ecology & Evolution 28: 156-166. doi:http://dx.doi.org/10.1016/j.tree.2012.10.002.
71. Boughman JW (2002) How sensory drive can promote speciation. Trends in Ecology and Evolution 17: 571-577.
72. Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: 'magic' but not rare? Trends in Ecology & Evolution 26: 389-397.