Polyandry reduces sperm length variation in social insects

Evolution

Volumn 65, Issue 10, 2011, Pages 3006-3012

  Fitzpatrick, John L ^a   Baer, Boris ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cryptic female choice; Postcopulatory sexual selection; Sperm competition; Sperm length; Sperm morphology

Indexed keywords

ANT; BEE; COPULATION; FEMALE BEHAVIOR; HYPOTHESIS TESTING; INTRASPECIFIC VARIATION; MORPHOLOGY; POLYANDRY; SEXUAL SELECTION; SOCIAL INSECT; SPERM; SPERM COMPETITION;

ANIMAL; ANT; ARTICLE; BEE; CYTOLOGY; FEMALE; MALE; MATE CHOICE; PHYLOGENY; PHYSIOLOGY; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SPERMATOZOON;

ANIMALS; ANTS; BEES; FEMALE; MALE; MATING PREFERENCE, ANIMAL; PHYLOGENY; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SPERMATOZOA;

APOIDEA; FORMICIDAE; HEXAPODA; INVERTEBRATA;

EID: 80053568922     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01343.x     Document Type: Article

References (59)

1. Anderson, M. J., J. Nyholt, and A. F. Dixson 2005. Sperm competition and the evolution of sperm midpiece volume in mammals. J. Zool. Lond. 267:135-142.
2. Bacci, M., Jr., S. E. Solomon, U. G. Mueller, V. G. Martins, A. O. R. Carvalho, L. G. E. Vieira, and A. C. O. Silva-Pinhati 2009. Phylogeny of leafcutter ants in the genus Atta Fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences. Mol. Phylogenet. Evol. 51:427-437.
3. Baer, B. 2003. Bumblebees as model organisms to study male sexual selection in social insects. Behav. Ecol. Sociobiol. 54:521-533.
4. Baer, B.. 2005. Sexual selection in Apis bees. Apidologie. 36:187-200.
5. Baer, B., and P. Schmid Hempel 2000. The artificial insemination of bumblebee queens. Insectes Soc. 47:183-187.
6. Baer, B., and J. J. Boomsma 2004. Male reproductive investment and queen mating frequency in fungus growing ants. Behav. Ecol. 15:426-432.
7. Baer, B., and J. J. Boomsma 2006. Mating biology of the leafcutting ants Atta colombica and A. cephalotes. J. Morphol. 267:1165-1171.
8. Baer, B., P. Schmid Hempel, J. T. Hoeg, and J. J. Boomsma 2003. Sperm length, sperm storage and mating system characteristics in bumblebees. Insectes Soc. 50:101-108.
9. Baer, B., M. B. Dijkstra, U. G. Mueller, D. R. Nash, and J. J. Boomsma 2009. Sperm length evolution in the fungus-growing ants. Behav. Ecol. 20:38-45.
10. Birkhead, T. R., and A. P. Møller, eds. 1998. Sperm competition and sexual selection. Academic Press, London, UK .
11. Birkhead, T. R., E. J. Pellatt, P. Brekke, R. Yeates, and H. Castillo-Juarez 2005. Genetic effects on sperm design in the zebra finch. Nature 434:383-387.
12. Birkhead, T. R., D. J. Hosken, and S. Pitnick, eds. 2009. Sperm biology: an evolutionary perspective. Academic, Burlington, MA .
13. Boomsma, J. J. 2007. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17:673-683.
14. Boomsma, J. J., B. Baer, and J. Heinze 2005. The evolution of male traits in social insects. Annu. Rev. Entomol. 50:395-420.
15. Breed, W. G., M. Bauer, R. Wade, N. Thitipramote, J. Suwajarat, and L. Yelland 2007. Intra-individual variation in sperm tail length in murine rodents. J. Zool. 272:299-304.
16. Briskie, J. V., and R. Montgomerie 1992. Sperm size and sperm competition in birds. Proc. R. Soc. Lond. B 247:89-95.
17. Briskie, J. V., R. Montgomerie, and T. R. Birkhead 1997. The evolution of sperm size in birds. Evolution 51:937-945.
18. Calhim, S., S. Immler, and T. R. Birkhead 2007. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2:e413.
19. den Boer, S. P. A., B. Baer, S. Dreier, S. Aron, D. R. Nash, and J. J. Boomsma 2009. Prudent sperm use by leaf-cutter ant queens. Proc. R. Soc. Lond. B 276:3945-3953.
20. den Boer, S. P. A., B. Baer, and J. J. Boomsma 2010. Seminal fluid mediates ejaculate competition in social insects. Science 327:1506-1509.
21. Eberhard, W. G. 1996. Female control: sexual selection by cryptic female choice. Princeton Univ. Press, Princeton, NJ .
22. Eddy, E. M. 2002. Male germ cell gene expression. Rec. Prog. Horm. Res. 57:103-128.
23. Fitzpatrick, J., R. Montgomerie, J. K. Desjardins, K. A. Stiver, N. Kolm, and S. Balshine 2009. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl Acad. Sci. USA 106:1128-1132.
24. Freckleton, R. P., P. H. Harvey, and M. Pagel 2002. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160:712-725.
25. Gage, M. J. G. 1994. Associations between body size, mating pattern, testis size and sperm length across butterflies. Proc. R. Soc. Lond. B 258:247-254.
26. Gomendio, M., and E. R. S. Roldan 2008. Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52:439-447.
27. Hunter, F. M., and T. R. Birkhead 2002. Sperm viability and sperm competition in insects. Curr. Biol. 12:121-123.
28. Hughes, W. O. H., B. P. Oldroyd, M. Beekman, and F. L. W. Ratnieks 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science. 320:1213-1216.
29. Immler, S. 2008. Sperm competition and sperm cooperation: the potential role of diploid and haploid expression. Reproduction 135:275-283.
30. Immler, S., and T. R. Birkhead 2007. Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proc. R. Soc. Lond. B 274:561-568.
31. Immler S., S. Calhim, and T. R. Birkhead 2008. Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538-1543.
32. Jamieson, B. G. M., R. Dallai, and B. A. Afzelius, eds. 1999. Insects: their spermatozoa and phylogeny. Scientific Publishers, Enfield, NH .
33. Joseph, S. B., and M. Kirkpatrick 2004. Haploid selection in animals. Trends Ecol. Evol. 19:592-597.
34. Kleven, O., T. Laskemoen, F. Fossøy, R. J. Robertson, and J. T. Lifjeld 2008. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62:494-499.
35. Malo, A. F., M. Gomendio, J. Garde, B. Lang-Lenton, A. J. Soler, and E. R. S. Roldan 2006. Sperm design and sperm function. Biol. Lett. 2:246-249.
36. Michalczyk, Ł., O. Y. Martin, A. L. Millard, B. C. Emerson, and M. J. G. Gage 2010. Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proc. R. Soc. Lond. B 277:3483-3491.
37. Miller, G. T., and S. Pitnick 2002. Sperm-female coevolution in Drosophila. Science 298:1230-1233.
38. Montgomerie R., and J. L. Fitzpatrick 2009. Testis size, sperm size and sperm competition. pp 1-53 in BGM Jamieson, ed. Reproductive biology and phylogeny of fishes, Science Publishers, Enfield, NH, pp 1-53.
39. Morrow, E. H., and M. J. G. Gage 2001. Consistent significant variation between individual males in spermatozoal morphometry. J. Zool. Lond. 254:147-153.
40. Nakagawa, S. 2004. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav. Ecol. 15:1044-1045.
41. Namekawa, S. H., P. J. Park, L.-F. Zhang, J. E. Shima, J. R. McCarrey, M. D. Griswold, and J. T. Lee 2006 Post- meiotic sex chromatin in the male germline of mice. Curr. Biol. 16:660-667.
42. Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
43. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. Camb. Philos. Soc. 45:525-567.
44. Parker, G. A.. 1993. Sperm competition games: sperm size and sperm number under adult control. Proc. R. Soc. Lond. B 253:245-254.
45. Parker, G. A., and M. E. Begon 1993. Sperm competition games: sperm size and number under gametic control. Proc. R. Soc. Lond. B 253:255-262.
46. Pitnick, S., D. J. Hosken, and T. R. Birkhead 2009a. Sperm morphological diversity. Pp 69-149 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology: an evolutionary perspective. Academic, Burlington, MA .
47. Pitnick, S., R. Dobler, and D. J. Hosken 2009b. Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria. Proc. R. Soc. Lond. B 276:4029-4034
48. Pizzari, T. and G. A. Parker 2009. Sperm competition and the sperm phenotype. Pp 207-245 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology: an evolutionary perspective. Academic, Burlington, MA .
49. Pizzari, T., and K. R. Foster 2008b. Sperm sociality: cooperation, altruism, and spite. PLoS Biol. 6:e130, 925-931.
50. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria .
51. Schultz, T. R., and S. G. Brady 2008. Major evolutionary transitions in ant agriculture. Proc. Natl. Acad. Sci. USA. 105:5435-5440.
52. Snook, R. R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20:46-53.
53. Suttle, J. M., A. D. M. Moore, E. J. Peirce, and W. G. Breed 1988. Quantitative studies on variation in sperm head morphology of the hopping mouse, Notomys alexis. J. Exp. Zool. 247:166-171.
54. Thitipramote, N., J. Suwanjarat, C. Leigh, and W. G. Breed 2010. Variation in sperm morphology of a murine rodent from South-East Asia: the Greater Bandicoot Rat, Bandicota indica. Acta Zoologica, doi: [Epub ahead of print].
55. Tomkins, J. L., and L. W. Simmons 2002. Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim. Behav. 63:1009-1016.
56. Tourmente, M., M. Gomendio, E. R. S. Roldan, L. Giojalas, and M. Chiaraviglio 2009. Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 63:2513-2524.
57. Tourmente, M., M. Gomendio, and E. R. S. Roldan 2011. Sperm competition and the evolution of sperm design in mammals. BMC Evolutionary Biology 11:12
58. Wang, P. J., J. R. McCarrey, F. Yang, and D. C. Page 2001. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27:422-426.
59. Ward, P. I. 1998. Intraspecific variation in sperm size characters. Heredity 80:655-659.