Does delayed fertilization facilitate sperm competition in bats?

Behavioral Ecology and Sociobiology

Volumn 67, Issue 12, 2013, Pages 1903-1913

  Orr, Teri J ^a,b   Zuk, Marlene ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Chiroptera; Delayed fertilization; Hibernation; Sexual selection; Sperm competition; Testes size

Indexed keywords

BAT; BODY SIZE; FEMALE; HIBERNATION; MUSEUM; REPRODUCTIVE CYCLE; SEXUAL SELECTION; SPERM COMPETITION;

CHIROPTERA; MAMMALIA;

EID: 84887619123     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-013-1598-2     Document Type: Article

References (91)

1. Amann RP (1970) Sperm production rates. In: Johnson AP, Gomes WR (eds) The testis. Academic Press, New York, pp 433-482.
2. Audet D, Thomas DW (1997) Facultative hypothermia as a thermoregulatory strategy in the phyllostomid bats, Carollia perspicillata and Sturnira lilium. J Comp Physiol B 167: 146-152.
3. Baker RJ, Clark CL (1987) Uroderma bilobatum. Mamm Species 279: 1-4.
4. Bernard RTF, Cumming GS (1997) African bats: evolution of reproductive patterns and delays. Q Rev Biol 72: 253-274.
5. Bernard RTF, Happold DCD, Happold M (1997) Sperm storage in a seasonally reproducing African vespertilionid, the banana bat (Pipistrellus nanus) from Malawi. J Zool 241: 161-174.
6. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446: 507-513.
7. Birkhead TR, Møller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50: 295-311.
8. Bradbury JW (1979) Behavioural aspects of reproduction in Chiroptera. J Reprod Fertil 56: 431-438.
9. Bradshaw G (1962) Reproductive cycle of the California leaf-nosed bat, Macrotus californicus. Science 136: 645-646.
10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, vol 2. Springer, New York.
11. Crichton EG (2000) Sperm storage and fertilization. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, London, pp 295-320.
12. Crichton EG, Seamark RF, Krutzsch PH (1989) The status of the corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay. Cell Tissue Res 258: 183-201.
13. Cryan PM, Jameson JW, Baerwald EF, Willis CKR, Barclay RMR, Snider EA, Crichton EG (2012) Evidence of late-summer mating readiness and early sexual maturation in migratory tree-roosting bats found dead at wind turbines. PLoS One 7: e47586.
14. Daniel JCJ (1970) Dormant embryos of mammals. Bioscience 20: 411-415.
15. DeFrees SL, Wilson DE (1988) Eidolon helvum. Mamm Species 312: 1-5.
16. Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119: 601-610.
17. Dietz M, Kalko EKV (2006) Seasonal changes in daily torpor patterns of free-ranging female and male Daubentońs bats (Myotis daubentonii). J Comp Physiol B 175: 1-9.
18. Dixson AF, Anderson MJ (2004) Sexual behavior, reproductive physiology and sperm competition in male mammals. Physiol Behav 83: 361-371.
19. Druecker JD (1972) Aspects of reproduction in Myotis volans, Lasionycteris noctivagans, and Lasiurus cinereus. Thesis University of New Mexico, Albuquerque.
20. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge, Massachusetts.
21. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton.
22. Fayenuwo JO, Halstead LB (1974) Breeding cycle of straw-colored fruit bat, Eidolon helvum, at Ile-Ife, Nigeria. J Mammal 55: 453-454.
23. Ferguson SH, Higdon JW, Larivière S (2006) Does seasonality explain the evolution and maintenance of delayed implantation in the family Mustelidae (Mammalia: Carnivora)? Oikos 114: 249-256.
24. Fleming TH (1971) Artibeus jamaicensis: delayed embryonic development in a neotropical bat. Science 171: 402-404.
25. Fleming TH, Hooper ET, Wilson DE (1972) Three central American bat communities: structure, reproductive cycles, and movement patterns. Ecology 53: 555-569.
26. Fox S, Spencer H, O'Brien GM (2008) Analysis of twinning in flying-foxes (Megachiroptera) reveals superfoetation and multiple-paternity. Acta Chiropterol 10: 271-278.
27. Funmilayo O (1979) Ecology of the straw-coloured fruit bat in Nigeria. Rev Zool Africaine 93: 589-600.
28. Garland T Jr, Bennett AF, Rezende EL (2005) Phylogenetic approaches in comparative physiology. J Exp Biol 208: 3015-3035.
29. Gartner GEA, Hicks JW, Manzani PR, Andrade DV, Abe AS, Wang T, Secor SM, Garland T Jr (2010) Phylogeny, ecology, and heart position in snakes. Physiol Biochem Zool 83: 43-54.
30. Gates WH (1936) Keeping bats in captivity. J Mammal 17: 268-272.
31. Geiser F, Stawski C (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr Comp Biol 51: 337-348.
32. Guthrie MJ (1933) The reproductive cycles of some cave bats. J Mammal 14: 199-216.
33. Hamilton I, Barclay RMR (1994) Patterns of daily torpor and day-roost selection by male and female big brown bats (Eptesicus fuscus). Can J Zool 72: 744-749.
34. Hayssen V, van Tienhoven A, van Tienhoven A (1993) Asdell's patterns of mammalian reproduction. Comstock Publishing Associates, Ithaca, NY.
35. Heckel G, von Helversen O (2002) Male tactics and reproductive success in the harem polygynous bat Saccopteryx bilineata. Behav Ecol 13: 750-756.
36. Heidman PD (1989) Delayed development in Fischer's pygmy fruit bat, Haplonycteris fischeri, in the Philippines. J Reprod Fertil 85: 363-382.
37. Hood CS, Smith JD (1989) Sperm storage in a tropical nectar-feeding bat, Macroglossus minimus (Pteropodidae). J Mammal 70: 404-406.
38. Hosken DJ (1997) Sperm competition in bats. Proc R Soc Lond B 264: 385-392.
39. Hosken DJ (1998a) Sperm fertility and skewed paternity during sperm competition in the Australian long-eared bat Nyctophilus geoffroyi (Chiroptera: Vespertilionidae). J Zool Lond 245: 93-100.
40. Hosken DJ (1998b) Testes mass in megachiropteran bats varies in accordance with sperm competition theory. Behav Ecol Sociobiol 44: 169-177.
41. Ives AR, Garland T Jr (2010) Phylogenetic logistic regression for binary dependent variables. Syst Biol 59: 9-26.
42. Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mammal 67: 1-22.
43. Krishna A, Dominic CJ (1983) Reproduction in the female short-nosed fruit bat Cynopterus sphinx. Period Biol 85: 23-30.
44. Krutzsch PH (1954) Notes on the habits of the bat, Myotis californicus. J Mammal 35: 539-545.
45. Krutzsch PH (1975) Reproduction of the canyon bat, Pipistrellus hesperus, in southwestern United States. Am J Anat 143: 163-200.
46. Krutzsch PH, Crichton EG, Nagle RB (1982) Studies on prolonged spermatozoa survival in Chiroptera: a morphological examination of storage and clearance of intrauterine and cauda epididymal spermatozoa in the bats Myotis lucifugus and M. velifer. Am J Anat 165: 421-434.
47. Kurta A, Kunz TH (1987) Size of bats at birth and maternal investment during pregnancy. Symp Zool Soc Lond 57: 79-106.
48. Lavin SR, Karsov WH, Ives AR, Middleton KM, Garland T Jr (2008) Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Phys Biochem Zool 81: 526-550.
49. Layne JN (1958) Notes on mammals of southern Illinois. Am Midl Nat 60: 219-254.
50. Lindenfors P, Dalen L, Angerbjörn A (2003) The monophyletic origin of delayed implantation in carnivores and its implications. Evolution 57: 1952-1956.
51. Lyman CP, Wimsatt WA (1966) Temperature regulation in the vampire bat, Desmodus rotundus. Physiol Zool 39: 101-109.
52. Martin PA, Reimers TJ, Lodge JR, Dzuik PJ (1974) The effect of ratios and number of spermatozoa mixed from two males on the proportion of offspring. J Reprod Fertil 39: 251-258.
53. McCracken GF, Wilkinson GS (2000) Bat Mating Systems. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, London, pp 321-362.
54. Miller-Butterworth CM, Murphy WJ, O'Brien SJ, Jacobs DS, Springer MS, Teeling EC (2007) A family matter: conclusive resolution of the taxonomic position of the long-fingered bats, Miniopterus. Mol Biol Evol 24: 1553-1561.
55. Mitchell GC (1965) A natural history study of the funnel-eared bat Natalus stramineus. Thesis University of Arizona, Tucson.
56. Mutere FA (1967) The breeding biology of equatorial vertebrates: reproduction in the fruit bat, Eidolon helvum, at latitude 0*20'N. J Zool Lond 153: 153-161.
57. Myers P (1977) Patterns of reproduction of four species of vespertilionid bats in Paraguay. Univ Calif Publ Zool 107: 1-41.
58. Neubaum DM, Wolfner MF (1999) Wise, winsome, or weird? Mechanisms of sperm storage in female animals. Curr Top Dev Biol 41: 67-97.
59. Okia O (1987) Reproductive cycles of East African bats. J Mammal 68: 138-141.
60. Orr RT (1954) Natural history of the pallid bat, Antrozous pallidus. Proc Calif Acad Sci 28: 165-264.
61. Orr TJ (2012) Doctoral dissertation. University of California, Riverside.
62. Ortega J, Castro-Arellano I (2001) Artibeus jamaicensis. Mamm Species 662: 1-9.
63. Ortega J, Maldonado JE, Wilkinson GS, Arita HT, Fleischer RC (2003) Male dominance, paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis). Mol Ecol 12: 2409-2415.
64. Oxberry BA (1979) Female reproductive patterns in hibernating bats. J Reprod Fertil 56: 359-367.
65. Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating Greater Horseshoe Bats (Rhinolophus ferrumequinum). Func Ecol 14: 580-588.
66. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45: 525-567.
67. Pearson OP, Koford MR, Pearson AK (1952) Reproduction of the lump-nosed bat (Corynorhinus rafinesquei) in California. J Mammal 33: 273-320.
68. Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, London, pp 69-149.
69. Quintero HF, Rasweiler JJ IV (1974) Ovulation and early embryonic development in the captive vampire bat, Desmodus rotundus. J Reprod Fertil 41: 265-273.
70. Racey PA (1974) The reproductive cycle in male noctule bats, Nyctalus noctula. J Reprod Fertil 41: 169-182.
71. Racey PA (1982) Ecology of bat reproduction. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 57-104.
72. Racey PA (2009) Reproductive assessment of bats. In: Kunz TH, Parsons P (eds) Ecological and behavioral methods for the study of bats, 2nd edn. The Johns Hopkins University Press, Baltimore, pp 249-264.
73. Racey PA, Entwistle AC (2000) Life-history and reproductive strategies of bats. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, London, pp 363-414.
74. Ramm S, Oliver P, Ponting CP, Stockley P, Emes RD (2008) Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol Biol Evol 25: 207-219.
75. Rasweiler JJ IV (1972) Reproduction in the long-tongued bat Glossophaga soricina. J Reprod Fertil 31: 249-262.
76. Rasweiler JJ IV, Badwaik NK (1997) Delayed development in the short-tailed fruit bat, Carollia perspicillata. J Reprod Fertil 109: 7-20.
77. Richardson EG (1977) The biology and evolution of the reproductive cycle of Miniopterus schreibersii and M. australis (Chiroptera: Vespertilionidae). J Zool 183: 353-375.
78. Rodrigues L, Ramos Pereira MJ, Rainho A, Palmeirim JM (2010) Behavioural determinants of gene flow in the bat Miniopterus schreibersii. Behav Ecol Sociobiol 64: 835-843.
79. Sandell M (1990) The evolution of seasonal delayed implantation. Q Rev Biol 65: 23-42.
80. Shump KA, Shump AU (1982) Lasiurus borealis. Mamm Species 183: 1-6.
81. Srivastava RK, Krishna A (2008) Seasonal adiposity, correlative changes in metabolic factors and unique reproductive activity in a vespertilionid bat, Scotphilus heathi. J Exp Zool 309A: 94-110.
82. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580-584.
83. Towers PA, Martin L (1985) Some aspects of female reproduction in the grey-headed flying-fox, Pteropus poliocephalus (Megachiroptera: Pteropodidae). Aust Mammal 8: 257-263.
84. Vonhof MJ, Barber D, Fenton MB, Strobeck C (2006) A tale of two siblings: multiple paternity in big brown bats (Eptesicus fuscus) demonstrated using microsatellite markers. Mol Ecol 15: 241-247.
85. Wai-Ping V, Fenton MB (1988) Nonselective mating in little brown bats (Myotis lucifugus). J Mammal 69: 641-645.
86. Webb PI, Speakman JR, Racey PA (1996) How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool 74: 761-765.
87. Wilde CJ, Knight CH, Racey PA (1999) Influence of torpor on milk protein composition and secretion in lactating bats. J Exp Zool 284: 35-41.
88. Wilkinson GS, McCracken GF (2003) Bats and balls: sexual selection and sperm competition in the Chiroptera. In: Kunz TH, Fenton MB (eds) Bat Ecology. University of Chicago Press, Chicago, pp 128-155.
89. Willis CKR, Brigham RM, Geiser F (2006) Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93: 80-83.
90. Wilson DE, LaVal RK (1974) Myotis nigricans. Mamm Species 39: 1-3.
91. Wimsatt WA (1960) Some problems of reproduction in relation to hibernation in bats. Bull Mus Comp Zool 124: 249-267.