Developmental environment effects on sexual selection in male and female Drosophila melanogaster

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Morimoto, Juliano ^a   Pizzari, Tommaso ^a   Wigby, Stuart ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; COVARIANCE; DROSOPHILA MELANOGASTER; EXPECTATION; EXPERIMENTAL MODEL; HUMAN; MATING; PATERNITY; PHENOTYPE; PRODUCTIVITY; PROGENY; SEXUAL SELECTION; SOCIAL ENVIRONMENT; ANIMAL; ENVIRONMENT; FEMALE; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; MATE CHOICE; PHYSIOLOGY; REPRODUCTION;

ANIMALS; DROSOPHILA MELANOGASTER; ENVIRONMENT; FEMALE; LARVA; MALE; MATING PREFERENCE, ANIMAL; REPRODUCTION;

EID: 84969801970     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0154468     Document Type: Article

References (82)

1. Andersson M. Sexual Selection. Princeton University Press. 1994.
2. Clutton-Brock T. Sexual Selection in Males and Females. Science. 2007; 318(5858):1882-5. doi: 10.1126/science.1133311 PMID: 18096798
3. Clutton-Brock T. Sexual selection in females. Anim Behav. 2009; 77(1):3-11.
4. Jones A. Validation of Bateman's principles: Comparative evidence from taxa with conventional and reversed sex roles. Integr Comp Biol. 2003; 43(6):834-. PMID: WOS:000222235200127.
5. Jones AG, Ratterman NL. Mate choice and sexual selection: what have we learned since Darwin? Proceedings of the National Academy of Sciences. 2009; 106 Suppl 1:10001-8. Epub 2009/06/17. doi: 10.1073/pnas.0901129106 PMID: 19528643; PubMed Central PMCID: PMC2702796.
6. Fritzsche K, Arnqvist G. Homage to Bateman: sex roles predict sex differences in sexual selection. Evolution. 2013; 67(7):1926-36. Epub 2013/07/03. doi: 10.1111/evo.12086 PMID: 23815650.
7. Knight J. Sexual stereotypes. Nature. 2002; 415(6869):254-6. PMID: 11796975
8. Cunningham EJA, Birkhead TR. Sex roles and sexual selection. Anim Behav. 1998; 56:1311-21. doi: 10.1006/Anbe.1998.0953 PMID: WOS:000078129400001.
9. Trivers RL. Parental investment and sexual selection. Biological Laboratories. 1972; 153.
10. Brown GR, Laland KN, Mulder MB. Bateman's principles and human sex roles. Trends Ecol Evol. 2009; 24(6-14):297-304. doi: 10.1016/j.tree.2009.02.005 PMID: PMC3096780.
11. Collet J, Richardson DS, Worley K, Pizzari T. Sexual selection and the differential effect of polyandry. Proceedings of the National Academy of Sciences. 2012; 109(22):8641-5. doi: 10.1073/Pnas.1200219109 PMID: WOS:000304881700059.
12. Collet JM, Dean RF, Worley K, Richardson DS, Pizzari T. The measure and significance of Bateman's principles. Proceedings of the Royal Society B-Biological Sciences. 2014; 281(1782). doi: 10.1098/rspb.2013.2973
13. Pelissie B, Jarne P, Sarda V, David P. Disentangling precopulatory and postcopulatory sexual selection in polyandrous species. Evolution. 2014; 68(5):1320-31. Epub 2014/01/15. doi: 10.1111/evo.12353 PMID: 24410424.
14. Parker GA, Pizzari T. Sexual selection: The logical imperative. Current Perspectives on Sexual Selection: Springer; 2015. p. 119-63.
15. Webster MS, PruettJones S, Westneat DF, Arnold SJ. Measuring the effects of pairing success, extrapair copulations and mate quality on the opportunity for sexual selection. Evolution. 1995; 49(6):1147-57. doi: 10.2307/2410439 PMID: WOS:A1995TR69500012.
16. Gerlach NM, McGlothlin JW, Parker PG, Ketterson ED. Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species. Behav Ecol. 2012; 23(5):1078-88. doi: 10.1093/beheco/ars077
17. Alonzo SH, Pizzari T. Male Fecundity Stimulation: Conflict and Cooperation Within and Between the Sexes: Model Analyses and Coevolutionary Dynamics. American Naturalist. 2010; 175(2):174-85. doi: 10.1086/649596 PMID: 20028216
18. Parker PG, Tang-Martinez Z. Bateman gradients in field and laboratory studies: a cautionary tale. Integrative Comparative Biology. 2005; 45(5):895-902. Epub 2005/11/01. doi: 10.1093/icb/45.5.895 PMID: 21676840.
19. Arnold SJ. Bateman Principles and the Measurement of Sexual Selection in Plants and Animals. American Naturalist. 1994; 144:S126-S49. doi: 10.1086/285656 PMID: WOS:A1994PA82600007.
20. Snyder BF, Gowaty PA. A reappraisal of Bateman's classic study of intrasexual selection. Evolution. 2007; 61(11):2457-68. Epub 2007/08/30. doi: 10.1111/j.1558-5646.2007.00212.x PMID: 17725639.
21. Worden BD, Parker PG. Polyandry in grain beetles, Tenebrio molitor, leads to greater reproductive success: material or genetic benefits? Behav Ecol. 2001; 12(6):761-7.
22. Ketterson ED, Parker PG, Raouf SA, Nolan V Jr, Ziegenfus C, Chandler CR. The relative impact of extra-pair fertilizations on variation in male and female reproductive success in dark-eyed juncos (Junco hyemalis). Ornithological Monographs. 1998:81-101.
23. Wedell N, Karlsson B. Paternal investment directly affects female reproductive effort in an insect. Proceedings of the Royal Society B-Biological Sciences. 2003; 270(1528):2065-71.
24. García-Navas V, Ferrer ES, Bueno-Enciso J, Barrientos R, Sanz JJ, Ortego J. Extrapair paternity in Mediterranean blue tits: socioecological factors and the opportunity for sexual selection. Behav Ecol. 2014; 25(1):228-38. doi: 10.1093/beheco/art111
25. Rowe L, Houle D. The lek paradox and the capture of genetic variance by condition dependent traits. Proceedings of the Royal Society B-Biological Sciences. 1996; 263(1375):1415-21. doi: 10.1098/Rspb.1996.0207 PMID: WOS:A1996VQ62200022.
26. Bonduriansky R. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev Camb Philos Soc. 2001; 76(3):305-39. Epub 2001/09/25. PMID: 11569787.
27. Cotton S, Small J, Pomiankowski A. Sexual selection and condition-dependent mate preferences. Curr Biol. 2006; 16(17):R755-65. Epub 2006/09/05. doi: 10.1016/j.cub.2006.08.022 PMID: 16950102.
28. Janicke T, David P, Chapuis E. Environment-Dependent Sexual Selection: Bateman's Parameters under Varying Levels of Food Availability. American Naturalist. 2015; 185(6):756-68. doi: 10.1086/681128 PMID: 25996861
29. Amitin EG, Pitnick S. Influence of developmental environment on male- and female-mediated sperm precedence in Drosophila melanogaster. J Evol Biol. 2007; 20(1):381-91. doi: 10.1111/J.1420-9101.2006.01184.X PMID: WOS:000242904600046.
30. Pitnick S, Garcia-Gonzalez F. Harm to females increases with male body size in Drosophila melanogaster. Proceedings of the Royal Society B-Biological Sciences. 2002; 269(1502):1821-8. doi: 10.1098/Rspb.2002.2090 PMID: WOS:000178004500011.
31. Lyimo E, Takken W, Koella J. Effect of rearing temperature and larval density on larval survival, age at pupation and adult size of Anopheles gambiae. Entomologia experimentalis et applicata. 1992; 63 (3):265-71.
32. Credland PF, Dick KM, Wright AW. Relationships between larval density, adult size and egg production in the cowpea seed beetle, Callosobruchus maculatus. Ecol Entomol. 1986; 11(1):41-50. doi: 10.1111/j.1365-2311.1986.tb00278.x
33. Honek A. Intraspecific Variation in Body Size and Fecundity in Insects - a General Relationship. Oikos. 1993; 66(3):483-92. doi: 10.2307/3544943 PMID: WOS:A1993KZ32600013.
34. Roff DA. Life history evolution: Sinauer Associates Sunderland; 2002.
35. Stearns SC. The evolution of life histories: Oxford University Press Oxford; 1992.
36. Wigby S, Perry JC, Kim YH, Sirot LK. Developmental environment mediates male seminal protein investment in Drosophila melanogaster. Funct Ecol. 2015; 30(3):410-9.
37. Hihara F. Effects of the male accessory gland secretion on oviposition and remating in females of Drosophila melanogaster. Zoological Magazine. 1981; 90(3):307-16.
38. Linklater JR, Wertheim B, Wigby S, Chapman T. Ejaculate depletion patterns evolve in response to experimental manipulation of sex ratio in Drosophila melanogaster. Evolution. 2007; 61(8):2027-34. Epub 2007/08/09. doi: 10.1111/j.1558-5646.2007.00157.x PMID: 17683443.
39. Sirot L, Buehner N, Fiumera A, Wolfner M. Seminal fluid protein depletion and replenishment in the fruit fly, Drosophila melanogaster: an ELISA-based method for tracking individual ejaculates. Behav Ecol Sociobiol. 2009; 63(10):1505-13. doi: 10.1007/s00265-009-0806-6 PMID: 24733957
40. Bangham J, Chapman T, Partridge L. Effects of body size, accessory gland and testis size on pre-and postcopulatory success in Drosophila melanogaster. Anim Behav. 2002; 64(6):915-21.
41. Zikovitz AE, Agrawal AF. The condition dependency of fitness in males and females: the fitness consequences of juvenile diet assessed in environments differing in key adult resources. Evolution. 2013; 67 (10):2849-60. Epub 2013/10/08. doi: 10.1111/evo.12170 PMID: 24094338.
42. Gillespie SR, Scarlett Tudor M, Moore AJ, Miller CW. Sexual selection is influenced by both developmental and adult environments. Evolution. 2014; 68(12):3421-32. Epub 2014/09/18. doi: 10.1111/evo.12526 PMID: 25226860.
43. Long TAF, Pischedda A, Stewart AD, Rice WR. A Cost of Sexual Attractiveness to High-Fitness Females. PLoS Biol. 2009; 7(12):e1000254. doi: 10.1371/journal.pbio.1000254 PMID: 19997646
44. Cornwallis CK, Uller T. Towards an evolutionary ecology of sexual traits. Trends Ecol Evol. 2010; 25 (3):145-52. http://dx.doi.org/10.1016/j.tree.2009.09.008. doi: 10.1016/j.tree.2009.09.008 PMID: 19853321
45. McGraw LA, Fiumera AC, Ramakrishnan M, Madhavarapu S, Clark AG, Wolfner MF. Larval rearing environment affects several post-copulatory traits in Drosophila melanogaster. Biol Lett. 2007; 3 (6):607-10. doi: 10.1098/Rsbl.2007.0334 PMID: WOS:000250903400006.
46. Pitnick S. Male Size Influences Mate Fecundity and Remating Interval in Drosophila-Melanogaster. Anim Behav. 1991; 41:735-45. doi: 10.1016/S0003-3472(05)80340-9 PMID: WOS: A1991FP02500001.
47. Lefranc A, Bundgaard J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas. 2000; 132(3):243-7. doi: 10.1111/J.1601-5223.2000.00243.X PMID: WOS:000089938200008.
48. Byrne PG, Rice WR. Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proceedings of the Royal Society B-Biological Sciences. 2006; 273(1589):917-22. Epub 2006/04/22. doi: 10.1098/rspb.2005.3372 PMID: 16627276; PubMed Central PMCID: PMC1560241.
49. Lüpold S, Manier MK, Ala-Honkola O, Belote JM, Pitnick S. Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behav Ecol. 2010:arq193.
50. Stubbs M. Density Dependence in the Life-Cycles of Animals and its Importance in K- and R-Strategies. J Anim Ecol. 1977; 46(2):677-88. doi: 10.2307/3837
51. Gage MJ. Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proceedings of the Royal Society B-Biological Sciences. 1995; 261(1360):25-30.
52. Lemaitre JF, Ramm SA, Hurst JL, Stockley P. Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal. Proceedings of the Royal Society B-Biological Sciences. 2011; 278(1709):1171-6. Epub 2010/10/01. doi: 10.1098/rspb.2010.1828 PMID: 20880887; PubMed Central PMCID: PMCPmc3049080.
53. Baldal EA, van der Linde K, van Alphen JJ, Brakefield PM, Zwaan BJ. The effects of larval density on adult life-history traits in three species of Drosophila. Mech Ageing Dev. 2005; 126(3):407-16. Epub 2005/01/25. doi: 10.1016/j.mad.2004.09.035 PMID: 15664627.
54. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, et al. Seminal Fluid Protein Allocation and Male Reproductive Success. Curr Biol. 2009; 19(9):751-7. doi: 10.1016/J.Cub.2009.03.036 PMID: WOS:000266131800027.
55. Fu W, Duan H, Frei E, Noll M. shaven and sparkling are mutations in separate enhancers of the Drosophila Pax2 homolog. Development. 1998; 125(15):2943-50. Epub 1998/07/10. PMID: 9655816.
56. Fricke C, Martin OY, Bretman A, Bussière LF, Chapman T. Sperm competitive ability and indices of lifetime reproductive success. Evolution. 2010; 64(9):2746-57. doi: 10.1111/j.1558-5646.2010.01022.x PMID: 20408874
57. Clancy DJ, Kennington WJ. A simple method to achieve consistent larval density in bottle cultures. Drosophila Information Service. 2001; 84:168-9.
58. Nilsen SP, Chan YB, Huber R, Kravitz EA. Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences. 2004; 101(33):12342-7. Epub 2004/08/11. doi: 10.1073/pnas.0404693101 PMID: 15302936; PubMed Central PMCID: PMC514477.
59. Tan CKW, Løvlie H, Pizzari T, Wigby S. No evidence for precopulatory inbreeding avoidance in Drosophila melanogaster. Anim Behav. 2012; 83(6):1433-41. http://dx.doi.org/10.1016/j.anbehav.2012.03.015.
60. Bjork A, Pitnick S. Intensity of sexual selection along the anisogamy-isogamy continuum. Nature. 2006; 441(7094):742-5. doi: 10.1038/Nature04683 PMID: WOS:000238095100052.
61. Zar JH. Biostatistical analysis: Pearson Education India; 1999.
62. Bohrnstedt GW, Goldberger AS. On the exact covariance of products of random variables. Journal of the American Statistical Association. 1969; 64(328):1439-42.
63. Seibold DR, McPhee RD. Commonality analysis: A method for decomposing explained variance in multiple regression analyses. Human Communication Research. 1979; 5(4):355-65.
64. Ray-Mukherjee J, Nimon K, Mukherjee S, Morris DW, Slotow R, Hamer M. Using commonality analysis in multiple regressions: a tool to decompose regression effects in the face of multicollinearity. Methods Ecol Evol. 2014; 5(4):320-8.
65. Rowell RK. Partitioning Predicted Variance into Constituent Parts: How To Conduct Commonality Analysis. 1991.
66. Lebigre C, Arcese P, Sardell RJ, Keller LF, Reid JM. Extra-pair paternity and the variance in male fitness in song sparrows (Melospiza melodia) Evolution. 2012; 66(10):3111-29. doi: 10.1111/j.1558-5646.2012.01677.x PMID: 23025602
67. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. 2010.
68. Chapman T, Partridge L. Female fitness in Drosophila melanogaster: An interaction between the effect of nutrition and of encounter rate with males. Proceedings of the Royal Society B-Biological Sciences. 1996; 263(1371):755-9. doi: 10.1098/Rspb.1996.0113 PMID: WOS:A1996UW13400013.
69. Prosser MR, Weatherhead PJ, Gibbs HL, Brown GP. Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon). Behav Ecol. 2002; 13(6):800-7. doi: 10.1093/beheco/13.6.800
70. Hosken DJ, Taylor ML, Hoyle K, Higgins S, Wedell N. Attractive males have greater success in sperm competition. Curr Biol. 2008; 18(13):R553-R4. doi: 10.1016/j.cub.2008.04.028 PMID: 18606122
71. Devigili A, Evans JP, Di Nisio A, Pilastro A. Multivariate selection drives concordant patterns of pre-and postcopulatory sexual selection in a livebearing fish. Nature communications. 2015; 6.
72. Manier MK, Belote JM, Berben KS, Novikov D, Stuart WT, Pitnick S. Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science. 2010; 328(5976):354-7. doi: 10.1126/science.1187096 PMID: 20299550
73. Pischedda A, Rice WR. Partitioning sexual selection into its mating success and fertilization success components. Proceedings of the National Academy of Sciences. 2012; 109(6):2049-53.
74. Eberhard WG. Copulatory Courtship and Cryptic Female Choice in Insects. Biol Rev Camb Philos Soc. 1991; 66(1):1-31. doi: 10.1111/J.1469-185x.1991.Tb01133.X PMID: WOS:A1991FB59700001.
75. García-González F, Simmons LW. Sperm viability matters in insect sperm competition. Curr Biol. 2005; 15(3):271-5. PMID: 15694313
76. Hunter F, Birkhead T. Sperm viability and sperm competition in insects. Curr Biol. 2002; 12(2):121-3. PMID: 11818062
77. Parker GA, Birkhead TR. Polyandry: the history of a revolution. Philosophical Transactions of the Royal Society B: Biological Sciences. 2013; 368(1613). doi: 10.1098/rstb.2012.0335
78. Edward DA, Chapman T. Measuring the fitness benefits of male mate choice in Drosophila melanogaster. Evolution. 2012; 66(8):2646-53. doi: 10.1111/j.1558-5646.2012.01648.x PMID: 22834761
79. Edward DA, Chapman T. Variation in Male Mate Choice in Drosophila melanogaster. PLoS One. 2013; 8(2):e56299. doi: 10.1371/journal.pone.0056299 PMID: 23405271
80. Trevitt S, Fowler K, Partridge L. An Effect of Egg-Deposition on the Subsequent Fertility and Remating Frequency of Female Drosophila-Melanogaster. J Insect Physiol. 1988; 34(8):821-8. doi: 10.1016/0022-1910(88)90157-6 PMID: WOS:A1988P555100011.
81. Jordan LA, Kokko H, Kasumovic M. Reproductive Foragers: Male Spiders Choose Mates by Selecting among Competitive Environments. American Naturalist. 2014; 183(5):638-49. doi: 10.1086/675755 PMID: 24739196
82. Edward DA, Fricke C, Gerrard DT, Chapman T. Quantifying the Life-History Response to Increased Male Exposure in Female Drosophila Melanogaster. Evolution. 2011; 65(2):564-73. doi: 10.1111/J.1558-5646.2010.01151.X PMID: WOS:000286629100020.