Battle and ballet: Molecular interactions between the sexes in drosophila

Journal of Heredity

Volumn 100, Issue 4, 2009, Pages 399-410

  Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Mating behavior; Proteolysis; Rapid evolution; Seminal proteins; Sequence conservation

Indexed keywords

ASTACIN; HORMONE PRECURSOR; LECTIN; OVULIN; PROTEIN ACP; PROTEINASE; SEMINAL PLASMA PROTEIN; UNCLASSIFIED DRUG;

CONFERENCE PAPER; CONTROLLED STUDY; DROSOPHILA; FEMALE; MALE; MATING; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN DEGRADATION; SEX DIFFERENCE; SPERM; SPERM PRESERVATION;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; METALLOPROTEASES; PEPTIDES; SEMEN; SEMINAL PLASMA PROTEINS; SEXUAL BEHAVIOR, ANIMAL; SPERM-OVUM INTERACTIONS;

ANIMALIA;

EID: 67650323690     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esp013     Document Type: Conference Paper

References (117)

1. Adams EM, Wolfner MF. 2007. Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage. J Insect Physiol. 53:319-331.
2. Aguadé M, Miyashita N, Langley C. 1992. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 132:755-770.
3. Aigaki T, Fleischmann I, Chen PS, Kubli E. 1991. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron. 7:557-563.
4. Allen AK, Spradling AC. 2008. The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development. 135:311-321.
5. Anderson RC. 1945. A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics. 30:280-296.
6. Andres JA, Maroja LS, Bogdanowicz SM, Swanson WJ, Harrison RG. 2006. Molecular evolution of seminal proteins in field crickets. Mol Biol Evol. 23:1574-1584.
7. Baer B, Boomsma JJ. 2006. Mating biology of the leaf-cutting ants Atta colombica and A. cephalotes. J Morphol. 267:1165-1171.
8. Bloch Qazi MC, Heifetz Y, Wolfner MF. 2003. The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. Dev Biol. 256:195-211.
9. Bode W, Gomis-Ruth FX, Huber R, Zwilling R, Stocker W. 1992. Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 358:164-167.
10. Braswell WE, Andres JA, Maroja LS, Harrison RG, Howard DJ, Swanson WJ. 2006. Identification and comparative analysis of accessory gland proteins in Orthoptera. Genome. 49:1069-1080.
11. Busso D, Cohen DJ, Da Ros V, Fissore R, Cuasnicu PS. 2003. Studies on the participation of epididymal sperm protein DE/CRISP-1 in egg activation. Cell Mol Biol. 49:407-412.
12. Carney GE, Taylor BJ. 2003. logjam encodes a predicted EMP24/GP25 protein that is required for Drosophila oviposition behavior. Genetics. 164:173-186.
13. Carvalho GB, Kapahi P, Anderson DJ, Benzer S. 2006. Allocrine modulation of appetite by the sex peptide of Drosophila. Curr Biol. 16:692-696.
14. Chapman T. 2001. Seminal fluid-mediated fitness traits in Drosophila. Heredity. 87:511-521.
15. Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, Smith HK, Partridge L. 2003. The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA. 100:9923-9928.
16. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-244.
17. Chen BX, Yuen ZX, Pan GW. 1985. Semen-induced ovulation in the bactrian camel (Camelus bactrianus). J Reprod Fertil. 74:335-339.
18. Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M, Bohlen P. 1988. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 54:291-298.
19. Chintapalli VR, Wang J, Dow JA. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 39: 715-720.
20. Civetta A, Singh RS. 1998. Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol. 15:901-909.
21. Clark AG, Aguadé M, Prout T, Harshman LG, Langley CH. 1995. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics. 139:189-201.
22. Clark AG, et al. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 450:203-218.
23. Clark NL, Aagaard JE, Swanson WJ. 2006. Evolution of reproductive proteins from animals and plants. Reproduction. 131:11-22.
24. Cohen DJ, Busso D, Da Ros V, Ellerman DA, Maldera JA, Goldweic N, Cuasnicu PS. 2008. Participation of cysteine-rich secretory proteins (CRISP) in mammalian sperm-egg interaction. Int J Dev Biol. 52:737-742.
25. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J. 2005. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem. 280:14948-14955.
26. Collins AM, Caperna TJ, Williams V, Garrett WM, Evans JD. 2006. Proteomic analyses of male contributions to honey bee sperm storage and mating. Insect Mol Biol. 15:541-549.
27. Da Ros V, Busso D, Cohen DJ, Maldera J, Goldweic N, Cuasnicu PS. 2007. Molecular mechanisms involved in gamete interaction: evidence for the participation of cysteine-rich secretory proteins (CRISP) in sperm-egg fusion. Soc Reprod Fertil Suppl. 65:353-356.
28. Da Ros VG, Maldera JA, Willis WD, Cohen DJ, Goulding EH, Gelman DM, Rubinstein M, Eddy EM, Cuasnicu PS. 2008. Impaired sperm fertilizing ability in mice lacking cysteine-rich secretory protein 1 (CRISP1). Dev Biol. 320:12-18.
29. Davies SJ, Chapman T. 2006. Identification of genes expressed in the accessory glands of male Mediterranean fruit flies (Ceratitis capitata). Insect Biochem Mol Biol. 36:846-856.
30. den Boer SPA, Boomsma JJ, Baer B. 2008. Seminal fluid enhances spermviability in the leafcutter ant Atta colombica. Behav Ecol Sociobiol.62:1843-1849.
31. DiBenedetto AJ, Lakich DM, Kruger WD, Belote JM, Baker BS, Wolfner MF. 1987. Sequences expressed sex-specifically in Drosophila melanogaster adults. Dev Biol. 119:242-251.
32. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156.
33. Dottorini T, Nicolaides L, Ranson H, Rogers DW, Crisanti A, Catteruccia F. 2007. A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc Natl Acad Sci USA. 104:16215-16220.
34. Eberhard WG. 1996. Female control: sexual selection by cryptic female choice. Princeton (NJ): Princeton University Press.
35. Fedorka KM, Linder JE, Winterhalter W, Promislow D. 2007. Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc Biol Sci. 274:1211-1217.
36. Findlay GD, Yi X, Maccoss MJ, Swanson WJ. 2008. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6:e178.
37. Fiumera AC, Dumont BL, Clark AG. 2005. Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics. 169:243-257.
38. Fiumera AC, Dumont BL, Clark AG. 2007. Associations between sperm competition and natural variation in male reproductive genes on the third chromosome of Drosophila melanogaster. Genetics. 176:1245-1260.
39. Fowler K, Partridge L. 1989. A cost of mating in female fruitflies. Nature. 338:760-761.
40. Gilbert DG. 1981. Ejaculate esterase and initial sperm use by female Drosophila melanogaster. J Insect Physiol. 27:641-650.
41. Gwathmey TM, Ignotz GG, Mueller JL, Manjunath P, Suarez SS. 2006. Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol Reprod. 75:501-507.
42. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, et al. 2007. Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics. 177:1321-1335.
43. Hall JC. 1994. The mating of a fly. Science. 264:1702-1714.
44. Han KA, Millar NS, Davis RL. 1998. A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci. 18:3650-3658.
45. He S, Lin YL, Liu YX. 1999. Functionally inactive protein C inhibitor in seminal plasma may be associated with infertility. Mol Hum Reprod. 5:513-519.
46. Heifetz Y, Lung O, Frongillo EA, Wolfner MF. 2000. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol. 10:99-102.
47. Heifetz Y, Vandenberg LN, Cohn HI, Wolfner MF. 2005. Two cleavage products of the Drosophila accessory gland protein ovulin can independently induce ovulation. Proc Natl Acad Sci USA. 102:743-748.
48. Heifetz Y, Wolfner MF. 2004. Seminal fluid and mating mediate changes in nerve termini innervating the Drosophila reproductive tract. Proc Natl Acad Sci USA. 101:6261-6266.
49. Herndon LA, Wolfner MF. 1995. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg-laying in females for one day following mating. Proc Natl Acad Sci USA. 92:10114-10118.
50. Ignotz GG, Lo MC, Perez CL, Gwathmey TM, Suarez SS. 2001. Characterization of a fucose-binding protein from bull sperm and seminal plasma that may be responsible for formation of the oviductal sperm reservoir. Biol Reprod. 64:1806-1811.
51. Jensen-Seaman MI, Li WH. 2003. Evolution of the hominoid semenogelin genes, the major proteins of ejaculated semen. J Mol Evol. 57:261-270.
52. Kaufmann BP, Demerec M. 1942. Utilization of sperm by the female Drosophila melanogaster. Am Nat. 76:445-469.
53. Kern AD, Jones CD, Begun DJ. 2004. Molecular population genetics of male accessory gland proteins in the Drosophila simulans complex. Genetics. 167:725-735.
54. Kise H, Nishioka J, Kawamura J, Suzuki K. 1996. Characterization of semenogelin II and its molecular interaction with prostate-specific antigen and protein C inhibitor. Eur J Biochem. 238:88-96.
55. Kubli E. 2003. Sex-peptides: seminal peptides of the Drosophila male. Cell Mol Life Sci. 60:1689-1704.
56. Langendijk P, Soede NM, Kemp B. 2005. Uterine activity, sperm transport, and the role of boar stimuli around insemination in sows. Theriogenology. 63:500-513.
57. Lawniczak MK, Begun DJ. 2004. A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome. 47: 900-910.
58. Liu H, Kubli E. 2003. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci USA. 100:9929-9933.
59. Lung O, Kuo L, Wolfner MF. 2001. Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. J Insect Physiol. 47:617-622.
60. Lung O, Tram U, Finnerty C, Eipper-Mains M, Kalb JM, Wolfner MF. 2002. The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. Genetics. 160:211-224.
61. Lung O, Wolfner MF. 1999. Drosophila seminal fluid proteins enter the circulatory system through the walls of the posterior vagina. Insect Biochem Mol Biol. 29:1043-1052.
62. Mack PD, Kapelnikov A, Heifetz Y, Bender M. 2006. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. Proc Natl Acad Sci USA. 103:10358-10363.
63. Magnusson WE. 1979. Production of an embryo by an Acrochordus javanicus isolated for 7 years. Copeia. 4:744-745.
64. Malm J, Hellman J, Hogg P, Lilja H. 2000. Enzymatic action of prostate-specific antigen (PSA or hK3): substrate specificity and regulation by Zn(2+), a tight-binding inhibitor. Prostate. 45:132-139.
65. Manning A. 1967. The control of sexual receptivity in female Drosophila. Anim Behav. 15:239-250.
66. McGraw LA, Gibson G, Clark AG, Wolfner MF. 2004. Genes regulated by mating, sperm or seminal proteins in mated female Drosophila melanogaster. Curr Biol. 14:1509-1514.
67. Monastirioti M. 2003. Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev Biol. 264:38-49.
68. Monsma SA, Harada HA, Wolfner MF. 1990. Synthesis of two Drosophila male accessory gland proteins and their fate after transfer to the female during mating. Dev Biol. 142:465-475.
69. Monsma SA, Wolfner MF. 1988. Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev. 2:1063-1073.
70. Moshitzky P, Fleischmann I, Chaimov N, Saudan P, Klauser S, Kubli E, Applebaum S. 1996. Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch Insect Biochem Physiol. 32:363-374.
71. Mueller JL, Linklater JR, Ravi Ram K, Chapman T, Wolfner MF. 2008. Targeted gene deletion and phenotypic analysis of the Drosophila melanogaster seminal fluid protease inhibitor Acp62F. Genetics. 178:1605-1614.
72. Mueller JL, Page JL, Wolfner MF. 2007. An ectopic expression screen reveals the protective and toxic effects of Drosophila seminal fluid proteins. Genetics. 175:777-783.
73. Mueller JL, Ravi Ram K, McGraw LA, Bloch Qazi MC, Siggia ED, Clark AG, Aquadro CF, Wolfner MF. 2005. Cross-species comparison of Drosophila male accessory gland protein genes. Genetics. 171:131-143.
74. Mueller JL, Ripoll DR, Aquadro CF, Wolfner MF. 2004. Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. Proc Natl Acad Sci USA. 101:13542-13547.
75. Murer V, Spetz JF, Hengst U, Altrogge LM, deAgostini A, Monard D. 2001. Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci USA. 98:3029-3033.
76. Neubaum DM, Wolfner MF. 1999a. Drosophila females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics. 153:845-857.
77. Neubaum DM, Wolfner MF. 1999b. Wise, winsome or wierd: mechanisms of sperm storage in female animals. (Schatten G and Pederson R, eds.). Curr Top Dev Biol. 41. 67-97.
78. O'Rand MG, Widgren EE, Wang Z, Richardson RT. 2006. Eppin: an effective target for male contraception. Mol Cell Endocrinol. 250:157-162.
79. Ottiger M, Soller M, Stocker RF, Kubli E. 2000. Binding sites of Drosophila melanogaster sex peptide pheromones. J Neurobiol. 44:57-71.
80. Panhuis TM, Clark NL, Swanson WJ. 2006. Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond B Biol Sci. 361:261-268.
81. Park M, Wolfner MF. 1995. Male and female cooperate in the processing of a Drosophila melanogaster seminal fluid protein. Dev Biol. 171:694-702.
82. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biol Revs. 45:525-567.
83. Peng J, Chen S, Busser S, Liu H, Honegger T, Kubli E. 2005a. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr Biol. 15:207-213.
84. Peng J, Zipperlen P, Kubli E. 2005b. Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr Biol. 15:1690-1694.
85. Peter A, Lilja H, Lundwall A, Malm J. 1998. Semenogelin I and semenogelin II, the major gel-forming proteins in human semen, are substrates for transglutaminase. Eur J Biochem. 252:216-221.
86. Pilpel N, Nezer I, Applebaum SW, Heifetz Y. 2008. Mating-increases trypsin in female Drosophila hemolymph. Insect Biochem Mol Biol. 38:320-330.
87. Pitnick S, Spicer GS, Markow TA. 1995. How long is a giant sperm? Nature 375:109.
88. Poiani A. 2006. Complexity of seminal fluid: a review. Behav Ecol Sociobiol. 60:289-310.
89. Prokupek A, Hoffmann F, Eyun SI, Moriyama E, Zhou M, Harshman L. 2008. An evolutionary expressed sequence tag analysis of Drosophila spermatheca genes. Evolution. 62:2936-2947.
90. Raina AK, Kingan TG, Giebultowicz JM. 1994. Mating-induced loss of sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantria dispar. Arch Insect Biochem Physiol. 25:317-327.
91. Ravi Ram K, Ji S, Wolfner MF. 2005. Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster. Insect Biochem Mol Biol. 35:1059-1071.
92. Ravi Ram K, Sirot LK, Wolfner MF. 2006. A predicted seminal astacin-like protease is required for the processing of reproductive proteins in Drosophila melanogaster. Proc Natl Acad Sci USA. 103:18674-18679.
93. Ravi Ram K, Wolfner MF. 2007a. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol. 47:427-445.
94. Ravi Ram K, Wolfner MF. 2007b. Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet. 3:e238.
95. Rice WR. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 381:232-234.
96. Riddiford LM. 1993. Hormones and Drosophila development. In: Bate M, Martinez AA, eds. The development of Drosophila melanogaster. Vol. 2. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory. p. 899-939.
97. Robert M, Gagnon C. 1999. Semenogelin I: a coagulum forming, multifunctional seminal vesicle protein. Cell Mol Life Sci. 55:944-960.
98. Robertson SA, Bromfield JJ, Tremellen KP. 2003. Seminal 'priming' for protection from pre-eclampsia - a unifying hypothesis. J Reprod Immunol. 59:253-265.
99. Schäfer U. 1986. Genes for male-specific transcripts in Drosophila melanogaster. Mol Gen Genet. 202:219-225.
100. Sirot LK, Poulson RL, Caitlin McKenna M, Girnary H, Wolfner MF, Harrington LC. 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol. 38:176-189.
101. Soller M, Bownes M, Kubli E. 1997. Mating and sex peptide stimulate the accumulation of yolk in oocytes of Drosophila melanogaster. Eur J Biochem. 243:732-738.
102. Soller M, Bownes M, Kubli E. 1999. Control of oocyte maturation in sexually mature Drosophila females. Dev Biol. 208:337-351.
103. Suarez SS. 2008. Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol. 52:455-462.
104. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA. 98:7375-7379. 00 Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144.
105. Tinbergen N. 1963. On aims and methods of ethology. Z Tierphysiol. 20:410-433.
106. Tsaur SC, Ting CT, Wu C-I. 1998. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol. 15:1040-1046.
107. Tsaur SC, Wu C-I. 1997. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol Biol Evol. 14:544-549.
108. Wagstaff BJ, Begun DJ. 2005. Molecular population genetics of accessory gland protein genes and testis-expressed genes in Drosophila mojavensis and D. arizonae. Genetics. 171:1083-1101.
109. Walker MJ, Rylett CM, Keen JN, Audsley N, Sajid M, Shirras AD, Isaac RE. 2006. Proteomic identification of Drosophila melanogaster male accessory gland proteins, including a pro-cathepsin and a soluble gamma-glutamyl transpeptidase. Proteome Sci. 4:9.
110. Weiss BL, Kaufman WR. 2004. Two feeding-induced proteins from the male gonad trigger engorgement of the female tick Amblyomma hebraeum. Proc Natl Acad Sci USA. 101:5874-5879.
111. Wigby S, Chapman T. 2005. Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol. 15:316-321.
112. Wigby S, Domanitskaya EV, Choffat Y, Kubli E, Chapman T. 2008. The effect of mating on immunity can be masked by experimental piercing in female Drosophila melanogaster. J Insect Physiol. 54:414-420.
113. Wolfner MF. 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol. 27:179-192. 00 Wolfner MF, Heifetz Y, Applebaum SW. 2005. Gonadal glands and their gene products. In: Gilbert LI, Iatrou K, Gil SS, eds. Comprehensive molecular insect science. Vol. 1. London: Elsevier. p. 179-212.
114. Wong A, Albright SN, Giebel JD, Ram KR, Ji S, Fiumera AC, Wolfner MF. 2008a. A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster. Genetics. 180:921-931.
115. Wong A, Turchin MC, Wolfner MF, Aquadro CF. 2008b. Evidence for positive selection on Drosophila melanogaster seminal fluid protease homologs. Mol Biol Evol. 25:497-506.
116. Yang CH, Belawat P, Hafen E, Jan LY, Jan YN. 2008. Drosophila egglaying site selection as a system to study simple decision-making processes. Science. 319:1679-1683.
117. Yapici N, Kim YJ, Ribeiro C, Dickson BJ. 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature. 451:33-37.