The developmental plasticity and functional significance of an additional sperm storage compartment in female yellow dung flies

Functional Ecology

Volumn 27, Issue 6, 2013, Pages 1392-1402

  Schäfer, Martin A ^a   Berger, David ^a,b   Jochmann, Ralf ^a   Blanckenhorn, Wolf U ^a   Bussière, Luc F ^c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Cryptic female choice; Cryptic genetic variation; Developmental constraint; Genetic canalization; Genital morphology; Phenotypic plasticity; Pleiotropy; Sperm competition

Indexed keywords

ENVIRONMENTAL CONDITIONS; FEMALE; FITNESS; FLY; GAMETE; GROWTH RATE; MULTIPLE MATING; PHENOTYPE; PHENOTYPIC PLASTICITY; PLASTICITY; PLEIOTROPY; SEXUAL SELECTION; SPERM; SPERM COMPETITION; SURVIVAL;

DIPTERA; SCATHOPHAGA STERCORARIA;

EID: 84887823169     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12134     Document Type: Article

References (81)

1. Abouheif, E. & Wray, G.A. (2002) Evolution of the gene network underlying wing polyphenism in ants. Science, 297, 249-252.
2. Amano, K. (1983) Studies on the intraspecific competition in dung-breeding flies 1. Effects of larval density on yellow dung fly, Scatophaga stercoraria L. (Diptera, Scatophagidae). Japanese Journal of Sanitary Zoology, 34, 165-175.
3. Amitin, E.G. & Pitnick, S. (2007) Influence of developmental environment on male- and female- mediated sperm precedence in Drosophila melanogaster. Journal of Evolutionary Biology, 20, 381-391.
4. Bächli, G. (1998) Family Drosophilidae. Contributions to a Manual of Palaearctic Diptera: Vol. 3 (eds L. Papp & B. Darvas ), pp. 503-513. Science Herald, Budapest.
5. Baminger, H. & Haase, M. (1999) Variation in spermathecal morphology and amount of sperm stored in populations of the simultaneously hermaphroditic land snail Arianta arbustorum. Journal of Zoology, 249, 165-171.
6. Bates, D., Maechler, M. & Bolker, B. (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-40. http://CRAN.R-project.org/package=lme4
7. Beese, K., Armbruster, G.F.J., Beier, K. & Baur, B. (2009) Evolution of female sperm-storage organs in the Carrefour of stylommatophoran gastropods. Journal of Zoological Systematics and Evolutionary Research, 47, 49-60.
8. Berger, D., Bauerfeind, S.S., Blanckenhorn, W.U. & Schäfer, M.A. (2011) High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution, 65, 2830-2842.
9. Berrigan, D. & Scheiner, S.M. (2004) Modelling the evolution of phenotypic plasticity. Phenotypic Plasticity: Functional and Conceptual Approaches (eds T. J. DeWitt & S. M. Scheiner ), pp. 82-97. Oxford University Press, Oxford.
10. Birkhead, T.R. (2010) How stupid not to have thought of that: post-copulatory sexual selection. Journal of Zoology, 281, 78-83.
11. Birkhead, T.R. & Møller, A.P. (1998) Sperm Competition and Sexual Selection. Academic Press, San Diego, CA.
12. Bjork, A., Starmer, W.T., Higginson, D.M., Rhodes, C.J. & Pitnick, S. (2007) Complex interactions with females and rival males limit the evolution of sperm offence and defence. Proceedings of the Royal Society B, 274, 1779-1788.
13. Blanckenhorn, W.U. (1998) Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. Evolution, 52, 1394-1407.
14. Blanckenhorn, W.U., Pemberton, A.J., Bussière, L.F., Römbke, J. & Floate, K.D. (2010) A review of the natural history and laboratory culture for the yellow dung fly, Scathophaga stercoraria (L.; Diptera: Scathophagidae). Journal of Insect Science, 10, article 11.
15. Bussière, L.F., Hunt, J.H., Stölting, K.N., Jennions, M.D. & Brooks, R. (2008) Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica, 134, 69-78.
16. Bussière, L.F., Demont, M., Pemberton, A.J., Hall, M.D. & Ward, P.I. (2010) The assessment of insemination success in yellow dung flies using competitive PCR. Molecular Ecology Resources, 10, 292-303.
17. Chase, B.A. & Baker, B.S. (1995) A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics, 139, 1649-1661.
18. Clark, A.G., Begun, D.J. & Prout, T. (1999) Female x male interactions in Drosophila sperm competition. Science, 283, 217-220.
19. De Jong, H. (2000) Family Scathophagidae. Contributions to a Manual of Palaearctic Diptera: Appendix (eds L. Papp & B. Darvas ), pp. 431-445. Science Herald, Budapest.
20. De Visser, J.A.G.M., Hermisson, J., Wagner, G.P., Meyers, L.A., Bagheri-Chaichian, H., et al. (2003) Evolution and detection of genetic robustness. Evolution, 57, 1959-1972.
21. Demont, M., Martin, O.Y. & Bussière, L.F. (2012) Wild yellow dung fly females may not select sperm based on dung pat microclimate but could nevertheless benefit from polyandry. Evolutionary Ecology, 26, 715-731.
22. Demont, M., Blanckenhorn, W.U., Hosken, D.J. & Garner, T.W.J. (2008) Molecular and quantitative genetic differentiation across Europe in yellow dung flies. Journal of Evolutionary Biology, 21, 1492-1503.
23. Dmitriew, C.M. (2011) The evolution of growth trajectories: what limits growth rate? Biological Reviews, 86, 97-116.
24. Dobzhansky, T. (1937) Genetics and the Origin of Species. Columbia University Press, New York, NY.
25. Eberhard, W.G. (1996) Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, Princeton, NJ.
26. Flatt, T. (2005) The evolutionary genetics of canalization. Quaterly Review of Biology, 80, 287-316.
27. Fox, J. & Weisberg, S. (2011) An {R} Companion to Applied Regression, 2nd edn. Sage, Thousand Oaks CA.
28. Gotthard, K. (2008) Adaptive growth decisions in butterflies. BioScience, 58, 222-230.
29. Gotthard, K. & Nylin, S. (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos, 74, 3-17.
30. Hadorn, E. & Garber, H. (1944) Über einen Drosophila-Stamm mit veränderten Spermatheken. Revue Suisse de Zoologie, 51, 418-423.
31. Haenni, J.P. (1997) Family Scathopsidae. Contributions to a Manual of Palaearctic Diptera: Vol. 2. (eds L. Papp & B. Darvas ), pp. 255-279. Science Herald, Budapest.
32. Hellriegel, B. & Bernasconi, G. (2000) Female-mediated differential sperm storage in a fly with complex spermathecae, Scatophaga stercoraria. Animal Behaviour, 59, 311-317.
33. Hellriegel, B. & Ward, P.I. (1998) Complex female reproductive tract morphology: its possible use in postcopulatory female choice. Journal of Theoretical Biology, 190, 179-186.
34. Higginson, D.M., Miller, K.B., Segraves, K.A. & Pitnick, S. (2012) Female reproductive tract form drives the evolution of complex sperm morphology. Proceedings of the National Academy of Sciences of the United States of America, 109, 4538-4543.
35. Hoekstra, H.E., Hirschmann, R.J., Bundey, R.J., Insel, P. & Crossland, J.P. (2006) A single aminoacid mutation contributes to adaptive color pattern in beach mice. Science, 313, 101-104.
36. Howard, D.J., Palumbi, S.R., Birge, L.M. & Manier, M.K. (2009) Sperm and speciation. Sperm Biology: An Evolutionary Perspective (eds T.R. Birkhead, D.J. Hosken & S. Pitnick ), pp. 368-403. Academic Press, London.
37. Hunt, J., Brooks, R. & Jennions, M.D. (2005) Female mate choice as a condition-dependent life-history trait. American Naturalist, 166, 79-92.
38. Jennions, M.D. & Petrie, M. (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews, 72, 283-327.
39. Jones, J.C. & Ludlam, K.W. (1965) Aedes aegypti with four spermathecae. Mosquito News, 25, 67-68.
40. Kamimura, Y. (2004) Mating behaviour and insemination in Diplatys flavicollis, an earwig with double-barrelled penises and a variable number of female sperm-storage organs. Journal of Zoology, 262, 37-46.
41. Koene, J.M. & Schulenburg, H. (2005) Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology, 5, article 25.
42. Kuntner, M., Coddington, J.A. & Schneider, J.M. (2009) Intersexual arms race? Genital coevolution in Nephild spiders (Araneae, Nephilidae). Evolution, 63, 1451-1463.
43. Mank, J.E. & Ellegren, H. (2009) Are sex-biased genes more dispensable? Biology Letters, 5, 409-412.
44. Mather, K. & Harrison, B.J. (1949) The manifold effect of selection part 2. Heredity, 3, 131-162.
45. Mayr, E. (1963) Animal Species and Evolution. Harward University Press, Cambridge, MA.
46. McLean, I.F.G. (1998) Family Chamaemyiidae. Contributions to a Manual of Palaearctic Diptera, Vol. 3 (eds L. Papp & B. Darvas ), pp. 415-423. Science Herald, Budapest.
47. Miller, G.T. & Pitnick, S. (2002) Sperm-female coevolution in Drosophila. Science, 298, 1230-1233.
48. Miller, G.T. & Pitnick, S. (2003) Functional significance of seminal receptacle length in Drosophila melanogaster. Journal of Evolutionary Biology, 16, 114-126.
49. Minder, A.M., Hosken, D.J. & Ward, P.I. (2005) Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). Journal of Evolutionary Biology, 18, 60-69.
50. Morrow, E.H., Pitcher, T.E. & Arnqvist, G. (2003) No evidence that sexual selection is an engine of speciation in birds. Ecology Letters, 6, 228-234.
51. Nakahara, M. & Tsubaki, Y. (2007) Function of multiple sperm-storage organs in female damselflies (Ischnura senegalensis): difference in amount of ejaculate stored, sperm loss, and priority in fertilization. Journal of Insect Physiology, 53, 1046-1054.
52. Otronen, M., Reguera, P. & Ward, P.I. (1997) Sperm storage in the yellow dung fly Scathophaga stercoraria: identifying the sperm of competing males in separate female spermathecae. Ethology, 103, 846-854.
53. Panhuis, T.M., Butlin, R., Zuk, M. & Tregenza, T. (2001) Sexual selection and speciation. Trends in Ecology and Evolution, 16, 364-371.
54. Pitnick, S., Markov, S.T.A. & Spicer, G.S. (1999) Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution, 53, 1804-1822.
55. Pitnick, S., Wolfner, M.F. & Suarez, S.S. (2009) Ejaculate-female and sperm-female interactions. Sperm Biology: An Evolutionary Perspective (eds T.R. Birkhead, D.J. Hosken & S. Pitnick ), pp. 247-304. Academic Press, London.
56. Presgraves, D.C., Baker, R.H. & Wilkinson, G.S. (1999) Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proceedings of the Royal Society B, 266, 1041-1047.
57. Puniamoorthy, N., Kotrba, M. & Meier, R. (2010) Unlocking the "black box": internal female genitalia in Sepsidae (Diptera) evolve fast and are species-specific. BMC Evolutionary Biology, 10, article 275.
58. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
59. Reinhardt, K., Harney, E., Naylor, R., Gorb, S. & Siva-Jothy, M.T. (2007) Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect. American Naturalist, 170, 931-935.
60. Römbke, J., Floate, K.D., Jochmann, R., Schäfer, M.A., Puniamoorthy, N., et al. (2009) Lethal and sublethal toxic effects of a test chemical (Ivermectin) on the yellow dung fly (Scatophaga stercoraria) based on a standardized international ring test. Environmental Toxicology & Chemistry, 28, 2117-2124.
61. Rönn, J., Katvala, M. & Arnqvist, G. (2007) Coevolution between harmful male genitalia and female resistance in seed beetles. Proceedings of the National Academy of Sciences of the United States of America, 104, 10921-10925.
62. Sbilordo, S.H., Schäfer, M.A. & Ward, P.I. (2009) Sperm release and use at fertilization by yellow dung fly females (Scathophaga stercoraria). Biological Journal of the Linnean Society, 98, 511-518.
63. Scharf, I., Bauerfeind, S.S., Blanckenhorn, W.U. & Schäfer, M.A. (2010) Effects of maternal and offspring environmental conditions on growth, development and diapause in latitudinal yellow dung fly populations. Climate Research, 43, 115-125.
64. Shapiro, M.D., Marks, M.E., Peichel, C.L., Blackman, B.K., Nereng, K.S., et al. (2004) Genetic and developmental basis of evolutionary pelvic reduction in three spine sticklebacks. Nature, 428, 717-723.
65. Simmons, L.W. (2001) Sperm Competition and its Evolutionary Consequences in the Insects. Princeton University Press, Princeton, NJ.
66. Simmons, L.W. (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annual Review of Ecology Evolution & Systematics, 36, 125-146.
67. Simmons, L.W. & Kotiaho, J.S. (2007) Quantitative genetic correlation between trait and preference supports a sexually selected sperm process in the beetle Onthophagus taurus. Proceedings of the National Academy of Sciences of the United States of America, 104, 16604-16608.
68. Simmons, L.W., Parker, G.A. & Stockley, P. (1999) Sperm displacement in the yellow dung fly, Scatophaga stercoraria: an investigation of male and female processes. American Naturalist, 153, 302-314.
69. Snow, L.S.E. & Andrade, M.C.B. (2005) Multiple sperm storage organs facilitate female control of paternity. Proceedings of the Royal Society B, 272, 1139-1144.
70. Sturtevant, A.H. (1925) The seminal receptacles and accessory glands of the Diptera, with special reference to the Acalyptera. Journal New York Entomological Society, 33, 195-215.
71. Thüler, K. (2009) The genetic architecture of female reproductive morphology and its influence on male and female life history in yellow dung flies Scathophaga stercoraria (L.). Doctoral thesis, University of Zurich, Zurich.
72. Tregenza, T., Attia, F. & Buahaiba, S.S. (2009) Repeatability and heritability of sperm competition outcomes in males and females of Tribolium castaneum. Behavioral Ecology & Sociobiology, 63, 817-823.
73. Tregenza, T., Wedell, N., Hosken, D.J. & Ward, P.I. (2003) Maternal effects on offspring depend on female mating pattern and offspring environment in yellow dung flies. Evolution, 57, 297-304.
74. Twig, E. & Yuval, B. (2005) Function of multiple sperm storage organs in female Mediterranean fruit flies (Ceratitis capitata, Diptera: Tephritidae). Journal of Insect Physiology, 51, 67-74.
75. Van Dyken, J.D. & Wade, M.J. (2010) The genetic signature of conditional expression. Genetics, 184, 557-570.
76. Waddington, C.H. (1953) Genetic assimilation of an acquired character. Evolution, 7, 118-126.
77. Ward, P.I. (2000) Female choice in the yellow dung fly Scathophaga stercoraria (L.). Evolution, 54, 1680-1686.
78. Ward, P.I. (2007) Postcopulatory selection in the yellow dung fly Scathophaga stercoraria (L.) and the mate-now-choose-later mechanism of cryptic female choice. Advances in the Study of Behavior, 37, 343-369.
79. Ward, P.I., Wilson, A.J. & Reim, C. (2008) A cost of female choice in the yellow dung fly. Genetica, 134, 63-67.
80. West-Eberhard, M. (2003) Developmental Plasticity and Evolution. Oxford University press, New York, NY.
81. Wexelson, H. (1928) Two new mutant characters on the spermathecae of the females of Drosophila melanogaster. Cell-degradation and supernumery spermathecae. Genetics, 13, 389-400.