Effects of simultaneous polyandry on offspring fitness in an African tree frog

Behavioral Ecology

Volumn 22, Issue 2, 2011, Pages 385-391

  Byrne, Phillip G ^a   Whiting, Martin J ^b,c  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

anuran amphibian; genetic benefits; offspring viability; polyandry; sexual selection

Indexed keywords

CLUTCH SIZE; FITNESS; FROG; GENETIC VARIATION; KIN RECOGNITION; LIFE HISTORY TRAIT; METAMORPHISM; POLYANDRY; SEXUAL SELECTION; SURVIVAL; WILD POPULATION;

AMPHIBIA; ANIMALIA; ANURA; CHIROMANTIS XERAMPELINA; HYLIDAE; VERTEBRATA;

EID: 79953855268     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/arq153     Document Type: Article

References (74)

1. Alford RA. 1999. Ecology: resource use, competition, and predation. In: McDiarmid RW, Altig R, editors. Tadpoles: the biology of anuran larvae. Chicago (Il): University of Chicago Press. p. 240-278.
2. Arnqvist G, Nilsson T. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav. 60:145-164.
3. Birkhead T. 1995. Sperm competition: evolutionary causes and consequences. Reprod Fertil Dev. 7:755-775.
4. Birkhead T. 2000. Promiscuity: an evolutionary history of sperm competition and sexual conflict. London: Faber and Faber.
5. Bradford DF, Seymour RS. 1988. Influence of water potential on growth and survival of the embryo and gas conductance of the egg, in a terrestrial breeding frog, Pseudophryne bibron. Physiol Zool. 61:470-474.
6. Brockmann HJ, Colson T, Potts W. 1994. Sperm competition in horseshoe crabs (Limulus polyphemus). Behav Ecol Sociobiol. 35:153-160. (Pubitemid 2136626)
7. Byrne PG, Keogh JS. 2009. Extreme sequential polyandry insures against nest failure in a frog. Proc R Soc Lond B Biol Sci. 276:115-120.
8. Byrne PG, Roberts JD. 2000. Does multiple paternity improve fitness of the frog Crinia georgiana? Evolution. 54:968-973. (Pubitemid 30466438)
9. Byrne PG, Roberts JD. 2004. Intrasexual selection and group spawning in quacking frogs (Crinia georgiana). Behav Ecol. 15:872-882. (Pubitemid 39147453)
10. Byrne PG, Whiting MJ. 2008. Simultaneous polyandry increases fertilization success in an African foam-nesting treefrog. Anim Behav. 76:1157-1164.
11. Curtsinger JW. 1991. Sperm competition and the evolution of multiple mating. Am Nat. 138:93-102.
12. D'Orgeix CA, Turner BJ. 1995. Multiple paternity in the red-eyed tree frog Agalychnis callidryas (Cope). Mol Ecol. 4:505-508.
13. Du Preez L, Carruthers V. 2009. A complete guide to the frogs of Southern Africa. Cape Town (South Africa): Struik.
14. Dziminski MA, Roberts JD, Simmons LW. 2008. Fitness consequences of parental compatibility in the frog Crinia georgiana. Evolution. 62:879-886. (Pubitemid 351489922)
15. Evans JP, Marshall DJ. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution. 59:106-112. (Pubitemid 40181303)
16. Forsman A, Ahnesjo J, Caesar S. 2007. Fitness benefits of diverse offspring in pygmy grasshoppers. Evol Ecol Res. 9:1305-1318. (Pubitemid 351224315)
17. Fox CW, Rauter CM. 2003. Bet-hedging and the evolution of multiple mating. Evol Ecol Res. 5:273-286. (Pubitemid 38681650)
18. Garcia-Gonzalez F, Simmons LW. 2005. The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J Evol Biol. 18:1097-1103. (Pubitemid 40968563)
19. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA. 2004. Spermatozoal traits and sperm competition in Atlantic salmon. Curr Biol. 14:44-47.
20. Halliday TR. 1998. Sperm competition and sexul selection in amphibians. In: Birkhead TR, Møller AP, editors. Sperm competition and sexual selection. London: Academic Press. p. 465-502.
21. Hosken DJ, Blanckenhorn WU. 1999. Female multiple mating, inbreeding avoidance, and fitness: it is not only the magnitude of costs and benefits that counts. Behav Ecol. 10:462-464. (Pubitemid 29456154)
22. Hosken DJ, Garner TWJ, Tregenza T, Wedell N, Ward PI. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Proc R Soc Lond Biol Sci. 2270:1933-1938.
23. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M. 2008. Ecological consequences of genetic diversity. Ecol Lett. 11: 609-623. (Pubitemid 351652095)
24. Ivy TM. 2007. Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses. J Evol Biol. 20:479-487.
25. Jennions MD, Backwell PRY, Passmore NI. 1992. Breeding behaviour of the African frog, Chiromantis xerampelina: multiple spawning and polyandry. Anim Behav. 44:1091-1100. (Pubitemid 23401707)
26. Jennions MD, Passmore NI. 1993. Sperm competition in frogs: testis size and a sterile male experiment on Chiromantis xerampelina (Rha-cophoridae). Biol J Linn Soc. 50:211-220.
27. Jennions MD, Petrie M. 2000. Why do females mate multiply? A review of the genetic benefits. Biol Rev. 75:21-64. (Pubitemid 30135849)
28. Kekäläinen J, Rudolfsen G, Janhunen M, Figenschou L, Peuhkuri N, Tamper N, Kortet R. 2010. Genetic and potential non-genetic benefits increase offspring fitness of polyandrous females in non-resource based mating system. BMC Evol Biol. 10:20.
29. Keller L, Reeve HK. 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav. 24: 291-315.
30. Konior M, Radwan J, Kolodziejczyk M. 2001. Polyandry increases offspring fecundity in the bulb mite. Evolution. 55:1893-1896. (Pubitemid 32984007)
31. Kusano T, Toda M, Fukuyama K. 1991. Testes size and breeding systems in Japanese anurans with special reference to large testes in the treefrog Rhacophorus arboreus (Amphibia: Rhacophoridae). Behav Ecol Sociobiol. 29:27-31.
32. Laurila A, Karttunen S, Merila J. 2002. Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution. 56:617-627. (Pubitemid 34299836)
33. Levins R. 1967. Evolution in changing environments. Princeton (NJ): Princeton University Press.
34. Levitan DR. 2002. The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution. 56:1599-1609.
35. Lips KR. 2001. Reproductive trade-offs and bet-hedging in Hyla calyp-sa, a neotropical treefrog. Oecologia. 128:509-518. (Pubitemid 32818357)
36. Marshall DJ, Evans JP. 2005. The benefits of polyandry in the free-spawning polychaete Galeolaria caespitosa. J Evol Biol. 18:735-741. (Pubitemid 40654095)
37. McCormick MI. 1999. Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia. 118: 412-422. (Pubitemid 29167413)
38. McLeod L, Marshall DJ. 2009. Do genetic diversity effects drive the benefits associated with multiple mating? A test in a marine invertebrate. PLoS One. 4:e6347.
39. McVey ME, Smittle BJ. 1984. Sperm precedence in the dragonfly Erythemis simplicicollis. J Insect Physiol. 30:619-628.
40. Metz EC, Kane RE, Yanagimachi H, Palumbi SR. 1994. Fertilization between closely related sea urchins is blocked by incompatabilities during sperm-egg attachment and early stages of fusion. Biol Bull. 187:23-34. (Pubitemid 2136879)
41. Mucina L, Rutherford MC, editors. 2006. The vegetation of South Africa, Lesotho and Swaziland. Pretoria (South Africa): South African National Biodiversity Institute.
42. Oliveira RF, Taborsky M, Brockmann HJ. 2008. Alternative reproductive tactics:an integrative approach. Cambridge: Cambridge University Press.
43. Pai AT, Yan GY. 2002. Polyandry produces sexy sons at the cost of daughters in red flour beetles. Proc R Soc Lond B Biol Sci. 269: 361-368.
44. Parker GA. 1970. Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. J Insect Physiol. 16:1301-1328.
45. Reichard M, Le Comber SC, Smith C. 2007. Sneaking from a female perspective. Anim Behav. 74:679-688. (Pubitemid 47538535)
46. Rice WR, Stewart AD, Morrow EH, Linder JE, Orteiza N, Byrne PG. 2006. Assessing sexual conflict in the Drosophila melanogaster laboratory model system. Philos Trans R Soc Lond B Biol Sci. 361:287-299. (Pubitemid 44870115)
47. Rowe L. 1992. Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Anim Behav. 44:189-202. (Pubitemid 23395357)
48. Seymour RS, Loveridge JP. 1994. Embryonic and larval respiration in the arboreal foam nests of the African frog Chiromantis xerampelina. J Exp Biol. 197:31-46.
49. Sheldon BC. 2000. Differential allocation: tests, mechanisms and implications. Trends Ecol Evol. 15:397-402.
50. Sherman CD, Wapstra HE, Olsson M. 2009. Consistent male-male paternity differences across female genotypes. Biol Lett. 5:232-234.
51. Sherman CD, Wapstra HE, Uller T, Olsson M. 2008a. Male and female effects on fertilization success and offspring viability in the Peron's tree frog, Litoria peronii. Austral Ecol. 33:348-352. (Pubitemid 351533703)
52. Sherman CD, Wapstra HE, Uller T, Olsson M. 2008b. Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii. Proc R Soc Lond B Biol Sci. 275:971-978. (Pubitemid 351323638)
53. Shine R, Harlow PS. 1996. Maternal manipulation of offspring phe-notypes via nest-site selection in an oviparous lizard. Ecology. 77:1808-1817.
54. Shvarts SS, Pyastolova OA. 1970. Regulators of growth and development of amphibian larvae. I. Specificity of effects. Soviet J Ecol. 1:58-62.
55. Simmons LW. 2005. The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann Rev Ecol Evol Syst. 36:125-146. (Pubitemid 43068853)
56. Simmons LW, Roberts JD, Dziminski MA. 2009. Egg jelly influences sperm motility in the externally fertilizing frog, Crinia georgiana. J Evol Biol. 22:225-229.
57. Sivinski J. 1984. Sexual conflict and choice in a phoretic fly, Borborillus frigipennis (Sphaeroceridae). Ann Ent Soc Am. 77:232-235.
58. Slatkin M. 1974. Competition and regional coexistence. Ecology. 55:128-134.
59. Taborsky M. 1998. Sperm competition in fish: 'bourgeois' males and parasitic spawning. Trends Ecol Evol. 13:222-227. (Pubitemid 28267762)
60. Telford SD, Jennions MD. 1998. Establishing cryptic female choice in animals. Trends Ecol Evol. 13:216-218.
61. Thom MD, Macdonald DW, Mason GJ, Pedersen V, Johnson PJ. 2004. Female American mink, Mustela vison, mate multiply in a free-choice environment. Anim Behav. 67:975-984. (Pubitemid 38617325)
62. Thornhill R. 1980. Rape in Panorpa scorpionflies and a general rape hypothesis. Anim Behav. 28:52-59.
63. Thumm K, Mahony M. 2002. Hatching dynamics and bet-hedging in a temperate frog, Pseudophryne australis (Anura: Myobatrachidae). Amphib-Reptil. 23:433-444. (Pubitemid 36257662)
64. Tregenza T, Wedell N. 1997. Natural selection bias? Nature. 386: 234-234.
65. Tregenza T, Wedell N. 2002. Polyandrous females avoid costs of inbreeding. Nature. 415:71-73. (Pubitemid 34062450)
66. Vacquier VD. 1998. Evolution of gamete recognition proteins. Science. 281:1995-1998. (Pubitemid 28475481)
67. Watson PJ. 1991. Multiple paternity as genetic bet-hedging in female Sierra dome spiders, Linyphia litigiosa (Linyphiidae). Anim Behav. 41:343-360.
68. Watson PJ. 1998. Multi-male mating and female choice increase offspring growth in the spider Neriene litigiosa (Linyphiidae). Anim Behav. 55:387-403. (Pubitemid 28166932)
69. Yasui Y. 1998. The 'genetic benefits' of female multiple mating reconsidered. Trends Ecol Evol. 13:246-250. (Pubitemid 28267767)
70. Zeh DW, Smith RL. 1985. Paternal investment by terrestrial arthropods. Am Zool. 25:785-805.
71. Zeh DW, Zeh JA, Bermingham E. 1997. Polyandrous, sperm-storing females: carriers of male genotypes through episodes of adverse selection. Proc R Soc Lond B Biol Sci. 264:119-125.
72. Zeh JA, Zeh DW. 1996. The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc Lond B Biol Sci. 263:1711-1717.
73. Zeh JA, Zeh DW. 1997. The evolution of polyandry 2. Post-copulatory defences against genetic incompatibility. Proc R Soc Lond B Biol Sci. 264:69-75.
74. Zeh JA, Zeh DW. 2008. Maternal inheritance, epigenetics and the evolution of polyandry. Genetica. 134:45-54.