Analysis of twinning in flying-foxes (Megachiroptera) reveals superfoetation and multiple-paternity

• Autorzy: Fox S. , Spencer H. , O'Brien G. M.
• Języki publikacji: EN

Abstrakty

EN

Published records of twinning and superfoetation in monotocous wild mammals are rare. Flying-foxes (Pteropodidae, Megachiroptera) occasionally produce twin offspring, fraternal twins, as well as superfoetation twins. Superfoetation occurs where a foetus is conceived when there is a foetus already developing. The resultant twins may be months apart in developmental stages so that one twin is usually born prematurely. Here, we review the current literature available on twinning and superfoetation in flying-foxes, and describe nine occurrences of multiple conceptions in Australian Pteropus species. Differences in sex and age of offspring clearly showed that most resulted from simultaneous or serial ovulations, not zygote splitting, thus excluding monozygous twinning. Additionally, an example of superfoetation is genetically analysed using six highly polymorphic microsatellite loci, to show multiple-paternity of superfoetation twins. Multiple births by flying-foxes are rare, leading the authors to conclude that the polyovulation constraint theory, found in the Microchiroptera, is not applicable in flying-foxes. The rare occurrence of additional ovulations do not usually produce additional live offspring. Post-ovulatory constraints, including the extra energetic demand twins place on a female flying-fox, are implicated in preventing successful production of multiple offspring.

Słowa kluczowe

EN

twinning; flying-fox zob.fruit bat; fruit bat; bat; Pteropus; twin; flying fox zob.fruit bat; Megachiroptera; superfoetation zob.superfetation; superfetation; multiple paternity

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2008
• Tom: 10
• Numer: 2
• Opis fizyczny: p.271-278,ref.

Twórcy

autor

Fox S.

• School of Marine and Tropical Biology, James Cook University, Townsville, 4811 QLD, Australia
• Wildlife Management Branch, Department of Primary Industries and Water, GPO Box 44, 7001 Hobart, Tasmania, Australia

autor

Spencer H.

• Cape Tribulation Tropical Research Station, RMB 5, Cape Tribulation, 4873 QLD, Australia

autor

O'Brien G. M.

• Department of Physiology, University of New England, Armidale, 2351 NSW, Australia

Bibliografia

• 1. R. M R. Barclay 1994. Constraints on reproduction by flying vertebrates: energy and calcium. American Naturalist 144:1021–1031. Google Scholar
• 2. R. M R. Barclay and L. D. Harder . 2003. Life histories of bats: life in the slow lane. Pp 209–256. in Bat ecology. T. H. Kunz and M. B. Fenton , editors. eds. University of Chicago Press. Chicago. 779. pp. Google Scholar
• 3. P. Eby 1991. Seasonal movements of grey-headed flying-foxes, Pteropus poliocephalus (Chiroptera: Pteropodidae) from two maternity camps in northern New South Wales. Wildlife Research 18:547–559. Google Scholar
• 4. P. Eby 1995. The biology and management of flying-foxes in New South Wales. Species Management Report, 18. New South Wales National Parks and Wildlife Service. Hurstville, Australia. viii +. 68. pp. Google Scholar
• 5. S. Fox, M. Waycott, and G. Dunshea . 2007. Isolation and characterisation of polymorphic microsatellite loci in the vulnerable spectacled flying fox, Pteropus conspicillatus. Conservation Genetics 8:1013–1016. Google Scholar
• 6. E. Girela, J. A. Lorente, J. C. Alvarez, M. D. Rodrigo, M. Lorente, and E. Villanueva . 1997. Indisputable double paternity in dizygous twins. Fertility and Sterility 67:1159–1161. Google Scholar
• 7. L. Hall and G. Richards . 2000. Flying-foxes: fruit and blossom bats of Australia. UNSW Press. Sydney. vi +. 135. pp. Google Scholar
• 8. K. Halpin, P. L. Young, H. E. Field, and J. S. Mackenzie . 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. Journal of General Virology 81:1927–1932. Google Scholar
• 9. V. Hayssen, A. van Tienhoven, and A. van Tienhoven . 1993. Asdell's patterns of mammalian reproduction: a compendium of species-specific data. Comstock Publishing Associates. Ithaca. 1,023. pp. Google Scholar
• 10. J. E. Hill 1941. A collection of mammals from Dondi, Angola. Journal of Mammalogy 22:81–85. Google Scholar
• 11. B. Khoshnood and B. Blondel . 2007. Regional variations in trends for multiple births: a population-based evaluation in France, 1972–2003. Twin Research and Human Genetics 10:406–415. Google Scholar
• 12. J. M. Laviree 1972. Superfetation chez une truie. Canadian Veterinary Journal 13:242–243. Google Scholar
• 13. T. C. Marshall, J. Slate, L. E B. Kruuk, and J. M. Pemberton . 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7:639–655. Google Scholar
• 14. L. Martin 1998. Posture and pauses during parturition in flying-foxes (genus Pteropus, suborder Megachiroptera). Australian Zoologist 30:437–442. Google Scholar
• 15. L. Martin, P. A. Towers, M. A. Mcguckin, L. Little, H. Luckhoff, and A. W. Blackshaw . 1987. Reproductive biology of flying-foxes (Chiroptera: Pteropodidae). Australian Mammalogy 10:115–118. Google Scholar
• 16. L. Martin, J. H. Kennedy, L. Little, H. C. Luckhoff, G. M. O'Brien, C. S T. Pow, P. A. Towers, A. K. Waldon, and D. Y. Wang . 1995. The reproductive biology of Australian flying-foxes (genus Pteropus). Symposium of the Zoological Society, London 67:167184. Google Scholar
• 17. N. Markus 2002. Behaviour of the black flying fox Pteropus alecto: 2. Territoriality and courtship. Acta Chiropterologica 4:153–166. Google Scholar
• 18. N. Markus and J. K. Blackshaw . 2002. Behaviour of the black flying fox Pteropus alecto: 1. An ethogram of behaviour, and preliminary characterisation of mather-infant inter actions. Acta Chiropterologica 4:137–152. Google Scholar
• 19. G. F. Mccracken and G. S. Wilkinson . 2000. Bat mating systems. Pp 141–154. in Reproductive biology of bats. E. G. Crichton and P. H. Krutzsch , editors. eds. Academic Press. London. 510. pp. Google Scholar
• 20. M. A. Mcguckin and A. W. Blackshaw . 1991. Seasonal changes in testicular size, plasma testosterone concentration and body weight in captive flying-foxes (Pteropus poliocephalus and P. scapulatus). Journal of Reproduction and Fertility 92:339–46. Google Scholar
• 21. J. E. Nelson 1965. Movements of Australian flying foxes (Pteropodidae: Megachiroptera). Australian Journal of Zoology 13:53–73. Google Scholar
• 22. G. M. O'Brien 1993. Seasonal reproduction in flying-foxes, reviewed in the context of other tropical mammals. Reproduction, Fertility and Development 5:499–521. Google Scholar
• 23. G. M. O'Brien and K. A. Gray . 2003. Central program and ovarian feedback both influence LH secretion in flyingfoxes. Proceedings of the Australian Physiological and Pharmacological Society 33:77P. Google Scholar
• 24. G. M. O'Brien and R. F. Nankervis . 1994. Coital behavior of male Pteropus scapulatus (little red flying foxes) in captivity. Physiology and Behavior 56:471–478. Google Scholar
• 25. G. M. O'Brien, J. D. Curlewis, and L. Martin . 1993. Effect of photoperiod on the annual cycle of testis growth in a tropical mammal, the little red flying-fox, Pteropus scapulatus. Journal of Reproduction and Fertility 98:121–27. Google Scholar
• 26. Z. Ozmen and A. Koker . 2004. Superfoetation and double parturition in an ewe. Indian Veterinary Journal 81:586–587. Google Scholar
• 27. G. Pison and A. V. D'Addato . 2006. Frequency of twin births in developed countries. Twin Research and Human Genetics 9:250–259. Google Scholar
• 28. M. P W. Platt, S. V. Glinianaia, J. Rankin, C. Wright, and M. Renwick . 2006. The north of England multiple pregnancy register: five-year results of data collection. Twin Research and Human Genetics 9:913–918. Google Scholar
• 29. A. L. Rand 1935. On the habits of some Madagascar mammals. Journal of Mammalogy 16:89–104. Google Scholar
• 30. W. S. Rasband 2004. ImageJ. U.S. National Institutes of Health. Bethesda, Maryland, USA. Google Scholar
• 31. J. Sambrook and D. W. Russell . 2001. Molecular cloning: a laboratory manual. 3rd editionCold Spring Harbour Laboratory Press. Cold Spring Harbour, N.Y. Google Scholar
• 32. L. A. Shilton, P. J. Latch, A. Mckeown, P. Pert, and D. A. Westcott . 2008. Landscape-scale redistribution of a highly mobile threatened species, Pteropus conspicillatus (Chiroptera, Pteropodidae), in response to tropical cyclone Larry. Austral Ecology 33:549–561. Google Scholar
• 33. A. D B. Smith 1927a. A case of superfoetation in the pig. Journal of Anatomy 61:329–332. Google Scholar
• 34. A. D B. Smith 1927b. Superfoetation — further cases in pigs and sheep. Journal of Anatomy 62:100–104. Google Scholar
• 35. G. Soudre, X. Guettier, L. Marpeau, L. Larue, T. Jault, and J. Barrat . 1992. In utero early suspicion of superfetation by ultrasound examination: a case report. Ultrasound in Obstetrics and Gynecology 2:51–54. Google Scholar
• 36. C. R. Tidemann 1999. The biology and management of the Grey-headed flying-fox, Pteropus poliocephalus. Acta Chiropterologica 1:151–164. Google Scholar
• 37. P. A. Towers and L. Martin . 1985. Some aspects of female reproduction in the grey-headed flying-fox, Pteropus poliocephalus (Megachiroptera: Pteropodidae). Australian Mammalogy 8:257–263. Google Scholar
• 38. M. L. Urquia, J. W. Frank, R. H. Glazier, and R. Moineddin . 2007. Multiple maternities and neighbourhood income. Twin Research and Human Genetics 10:400–405. Google Scholar
• 39. M. J. Vardon and C. R. Tidemann . 1998. Reproduction, growth and maturity in the black flying-fox, Pteropus alecto (Megachiroptera: Pteropodidae). Australian Journal of Zoology 46:329–344. Google Scholar
• 40. W. A. Wimsatt 1979. Reproductive asymmetry and unilateral pregnancy in Chiroptera. Journal of Reproduction and Fertility 56:345–357. Google Scholar
• 41. J. Worthington-Wilmer and E. Barratt . 1996. A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Research News 37:1–3. Google Scholar
• 42. N. Yamaguchi, R. J. Sarno, W. E. Johnson, S. J. O'Brien, and D. W. Macdonald . 2004. Multiple paternity and reproductive tactics of free-ranging American minks, Mustela vison. Journal of Mammalogy 85:432–439. Google Scholar