Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies

Evolution

Volumn 65, Issue 10, 2011, Pages 2843-2854

  Estrada, Catalina ^a,c   Schulz, Stefan ^b   Yildizhan, Selma ^b   Gilbert, Lawrence E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

Female mating receptivity; Heliconius; Male control on female reproduction; Male male competition; Sexual conflict; Signal evolution

Indexed keywords

PHEROMONE;

BUTTERFLY; DIVERGENCE; PHEROMONE; PHYLOGENETICS; POLYANDRY; REPRODUCTIVE STRATEGY; SEXUAL SELECTION; SIGNAL;

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; BUTTERFLY; CHEMISTRY; EVOLUTION; FEMALE; GENETICS; MALE; MATE CHOICE; PHYSIOLOGY;

ANIMAL COMMUNICATION; ANIMALS; BIOLOGICAL EVOLUTION; BUTTERFLIES; FEMALE; MALE; MATING PREFERENCE, ANIMAL; PHEROMONES;

HELICONIUS; PAPILIONOIDEA;

EID: 80053461419     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01352.x     Document Type: Article

References (80)

1. Andersson, J., A. K. Borg-Karlson, and C. Wiklund 2000. Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc. R .Soc. Lond. B 267:1271-1275.
2. Andersson, J., A. K. Borg-Karlson, and C. Wiklund 2003. Antiaphrodisiacs in pierid butterflies: a theme with variation! J. Chem. Ecol. 29:1489-1499.
3. Andersson, J., A. K. Borg-Karlson, and C. Wiklund 2004. Sexual conflict and anti-aphrodisiac titre in a polyandrous butterfly: male ejaculate tailoring and absence of female control. Proc. R. Soc. Lond. B. 271:1765-1770.
4. Arak, A., and M. Enquist 1995. Conflict, receiver bias and the evolution of signal form. Philos. Trans. R. Soc. Lond. B 349:337-344.
5. Arnqvist, G. 1998. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393:784-785.
6. Arnqvist, G., and T. Nilsson 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60:145-164.
7. Arnqvist, G., and L. Rowe 2005. Sexual conflict. Princeton Univ. Press, Princeton, NJ
8. Ayasse, M., R. J. Paxton, and J. Tengö 2001. Mating behavior and chemical communication in the order Hymenoptera. Annu. Rev. Entomol. 46:31-78.
9. Bateman, P. W., J. W. H. Ferguson, and C. A. Yetman 2006. Courtship and copulation, but not ejaculates, reduce the longevity of female field crickets (Gryllus bimaculatus). J. Zool. (Lond) 268:341-346.
10. Beltrán, M., C. D. Jiggins, A. V. Z. Brower, E. Bermingham, and J. L. B. Mallet 2007. Do pollen feeding, pupal mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biol. J. Linn. Soc. 92:221-239.
11. Bissoondath, C. J., and C. Wiklund 1997. Effect of male body size on sperm precedence in the polyandrous butterfly Pieris napi L. (Lepidoptera: Pieridae). Behav. Ecol. 8:518-523.
12. Boggs, C. L. 1979. Resource allocation and reproductive strategies in several Heliconiine butterfly species. Univ. of Texas, Austin
13. Boggs, C. L. 1990. A general model of the role of male-donated nutrients in female insects' reproduction. Am. Nat. 136:598-617.
14. Boggs, C. L., and L. E. Gilbert 1979. Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83-84.
15. Bradbury, J. W., and S. L. Vehrencamp 1998. Principles of animal communication. Sinauer Associates, Inc., Sunderland, MA
16. Brown, K. S. 1981. The biology of Heliconius and related genera. Annu. Rev. Entomol. 26:427-457.
17. Cardé, R. T., and K. F. Haynes 2004. Structure of the pheromone communication channel in moths in R. T. Cardé, and J. G. Millar, eds. Advances in insect chemical ecology. Univ. Press, Cambridge
18. Chapman, T. 2001. Seminal fluid-mediated fitness traits in Drosophila. Heredity 87:511-521.
19. Chapman, T., and S. J. Davies 2004. Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides 25:1477-1490.
20. Deinert, E. I., J. T. Longino, and L. E. Gilbert 1994. Mate competition in butterflies. Nature 370:23-24.
21. Eltringham, M. A. 1925. On the abdominal glands in Heliconius (Lepidoptera). Trans. Entomol. Soc. Lond. 269-275.
22. Estrada, C. 2009. Sexual behavior, intraspecific signaling and the evolution of mimicry among closely related species. Univ. of Texas, Austin
23. Estrada, C., and C. D. Jiggins 2002. Patterns of pollen feeding and habitat preference among Heliconius species. Ecol. Entomol. 27:448-456.
24. Estrada, C., S. Yildizhan, S. Schulz, and L. E. Gilbert 2010. Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proc. R. Soc. Lond. B. 277:407-413.
25. Farris, J. S. 1989. The retention index and homoplasy excess. Syst. Biol. 38:406-407.
26. Forsberg, J., and C. Wiklund 1989. Mating in the afternoon: time saving in courtship and remating by females of a polyandrous butterfly Pieris napi L. Behav. Ecol. Sociobiol. 25:349-356.
27. Fatouros, N. E., M. E. Huigens, J. J. A. vanLoon, M. Dicket, and M. Hilker 2005. Butterfly anti-aphrodisiac lures parasitic wasps. Nature. 433:704.
28. Fatouros, N. E., C. Broekgaarden, G. Bukovinszkine'Kiss, J. J. A. van Loon, R. Mumm, M. E. Huigens, M. Dicke, and M. Hilker 2008. Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense. Proc. Natl. Acad. Sci. USA 105:10033-10038.
29. Fourment, M., and M. J. Gibbs 2006. PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol. Biol. 6:1.
30. Gilbert, L. E. 1976. Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? Science 193 419-420.
31. Gilbert, L. E. 2003. Adaptive novelty through introgression in Heliconius wing patterns: evidence for a shared genetic 'toolbox' from synthetic hybrid zones and a theory of diversification. Pp. 281-318 in C. L. Boggs, W. Watt, and P. R. Ehrlich, eds. Ecology and evolution taking flight: butterflies as model study systems. Univ. of Chicago Press, Chicago
32. Haerty, W., S. Jagadeeshan, R. J. Kulathinal, A. Wong, K. Ravi Ram, L. K. Sirot, L. Levesque, C. G. Artieri, M. F. Wolfner, A. Civetta, and R. S. Singh 2007. Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321-1335.
33. Happ, G. 1969. Multiple sex pheromones of the mealworm beetle, Tenebrio molitor L. Nature 222:180-181.
34. Jetz, W., C. Rowe, and T. Guilford 2001. Non-warning odors trigger innate color aversions-as long as they are novel. Behav. Ecol. 12:134-139.
35. Kluge, A. G., and J. S. Farris 1969. Quantitative phyletics and the evolution of anurans. Syst. Zool. 18:1-32.
36. Kronforst, M. R., L. G. Young, D. D. Kapan, C. McNeely, R. J. O'Neill, and L. E. Gilbert 2006. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc. Natl. Acad. Sci. USA 103:6575-6580.
37. Kronforst, M. R. 2008. Gene flow persists millions of years after speciation in Heliconius butterflies. BMC Evol. Biol. 8:98.
38. Maddison, W. P., and D. R. Maddison 2008. Mesquite: a modular system for evolutionary analysis. Version 2.5.
39. Maddison, W. P., and M. Slatkin 1991. Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45:1184-1197.
40. Mallet, J. L. B., and L. E. Gilbert 1995. Why are there so many mimicry rings? Correlation between habitat, behavior and mimicry in Heliconius butterflies. Biol. J. Linn. Soc. 55:159-180.
41. Mallet, J. L. B., M. Beltrán, W. Neukirchen, and M. Linares 2007. Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evol. Biol. 7:28.
42. McCracken, K. G., and F. H. Sheldon 1997. Avian vocalizations and phylogenetic signal. Proc. Natl. Acad. Sci. USA 94:3833-3836.
43. Mendoza-Cuenca, L., and R. Macías-Ordóñez 2005. Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioral compensation. J. Trop. Ecol. 21:407-415.
44. Moore, B. P., and W. V. Brown 1989. Graded levels of chemical defence in mimics of lycid beetles of the genus Metmorrhynchus (Coleoptera). Aust. J. Entomol. 28:229-233.
45. Moore, B. P., W. V. Brown, and M. Rothschild 1990. Methylalkylpyrazines in aposematic insects, their hostplants and mimics. Chemoecology 1:43-51.
46. Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47:57-92.
47. Ord, T. J., and E. P. Martins 2006. Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Anim. Behav. 71:1411-1429.
48. Päckert, M., J. Martens, J. Kosuch, A. A. Nazarenko, and M. Veith 2003. Phylogenetic signal in the song of crests and kinglets (Aves: Regulus). Evolution 57:616-629.
49. Raffa, K., K. Hobson, S. LaFontaine, and B. Aukema 2007. Can chemical communication be cryptic? Adaptations by herbivores to natural enemies exploiting prey semiochemistry. Oecologia 153:1009-1019.
50. Ross, P., and D. Crews 1977. Influence of the seminal plug on mating behaviour in the garter snake. Nature 267:344-345.
51. Ross, G. N., H. M. Fales, H. A. Lloyd, T. Jones, E. A. Sokoloski, K. Marshall-Batty, and M. S. Blum 2001. Novel chemistry of abdominal defensive glands of Nymphalid butterfly Agraulis vanillae. J. Chem. Ecol. 27:1219-1228.
52. Rowe, C., and T. Guilford 1999. The evolution of multimodal warning displays. Evol. Ecol. 13:655-671.
53. Ryan, M. J., and A. S. Rand 1995. Female responses to ancestral advertisement calls in túngara frogs. Science 269:390-392.
54. Sanderson, M., and M. J. Donoghue 1989. Patterns of variation in levels of homoplasy. Evolution 43:1781-1795.
55. Schulz, S., M. Boppré, and R. I. Vane-Wright 1993. Specific mixtures of secretions from male scent organs of African milkweed butterflies (Danainae). Philos. Trans. R. Soc. Lond. B 342:161-181.
56. Schulz, S., S. Yildizhan, K. Stritzke, C. Estrada, and L. E. Gilbert 2007. Macrolides from the scent glands of the tropical butterflies Heliconius cydno and Heliconius pachinus. Org. Biomol. Chem. 5:3434-3441.
57. Schulz, S., C. Estrada, S. Yildizhan, M. Boppré, and L. Gilbert 2008. An antiaphrodisiac in Heliconius melpomene butterflies. J. Chem. Ecol. 34:82-93.
58. Scott, D. 1986. Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. Proc. Natl. Acad. Sci. USA 83:8429-8433.
59. Scott, D., and L. L. Jackson 1988. Interstrain comparison of male-predominant antiaphrodisiacs in Drosophila melanogaster. J. Insect Physiol. 34:863-871.
60. Siddall, E. C., and N. M. Marples 2008. Better to be bimodal: the interaction of color and odor on learning and memory. Behav. Ecol. 19:425-432.
61. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects Princeton Univ. Press, Princeton and Oxford
62. Solensky, M. J., and K. S. Oberhauser 2009. Sperm precedence in monarch butterflies (Danaus plexippus). Behav. Ecol. 20:328-334.
63. Srygley, R., and C. P. Ellington 1999. Discrimination of flying mimetic, passion-vine butterflies Heliconius Proc. R. Soc. Lond. B 266:2137-2140.
64. Stowe, M. K., T. C. J. Turlings, J. H. Loughrin, W. J. Lewis, and J. H. Tumlinson 1995. The chemistry of eavesdropping, alarm, and deceit. Proc. Natl. Acad. Sci. USA 92:23-28.
65. Sullivan, J. P., S. Lavoué, and C. D. Hopkins 2000. Molecular systematics of the African electric fishes (Mormyroidea: Teleostei) and a model for the evolution of their electric organs. J. Exp. Biol. 203:665-683.
66. Swofford, D. L. 2002. PAUP* Phylogenetic analysis using parsimony. version 4.0b10 for 32-bit Microsoft Windows., Florida State Univ., Tallahassee, FL
67. Symonds, M. R. E., and M. A. Elgar 2004. The mode of pheromone evolution: evidence from bark beetles. Proc. R. Soc. Lond. B 271:839-846.
68. Symonds, M. R. E., and M. A. Elgar 2008. The evolution of pheromone diversity. Trends Ecol. Evol. 23:220-228.
69. Symonds, M. R. E., and B. Wertheim 2005. The mode of evolution of aggregation pheromones in Drosophila species. J. Evol. Biol. 18:1253-1263.
70. Thornhill, R., and J. Alcock 1983. The evolution of insect mating systems. Harvard Univ. Press, Cambridge, MA
71. Wagstaff, B. J., and D. J. Begun 2005. Molecular population genetics of accessory gland protein genes and testis-expressed genes in Drosophila mojavensis and D. arizonae. Genetics 171:1083-1101.
72. Wagstaff, B. J., and D. J. Begun 2007. Adaptive evolution of recently duplicated accessory gland protein genes in desert Drosophila. Genetics 177:1023-1030.
73. Walters, J. R., and R. G. Harrison 2010. Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. Mol. Biol. Evol. 27:2000-2013.
74. Wedell, N. 2005. Female receptivity in butterflies and moths. J. Exp. Biol. 208:3433-3440.
75. Wiklund, C. 2003. Sexual selection and the evolution of butterfly mating systems. Pp. 67-90 in C. L. Boggs, W. B. Watt, and P. R. Ehrlich, eds. Butterflies: ecology and evolution taking flight. Univ. of Chicago Press, Chicago
76. Wiklund, C., B. Karlsson, and O. Leimar 2001. Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proc. R. Soc. Lond. B 268:1661-1667.
77. Wiklund, C., K. Gotthard, and S. Nylin 2003. Mating system and the evolution of sex-specific mortality rates in two nymphalid butterflies. Proc. R. Soc. Lond. B 270:1823-1828.
78. Willett, P., J. M. Barnard, and G. M. Downs 1998. Chemical similarity searching. J. Chem. Inf. Comput. Sci. 38:983-996.
79. Yildizhan, S. 2009. Die Komplexität chemischer Signalsysteme bei männlichen Lepidopteren. Technischen Univesrität Carolo-Wilhelmina zu Braunschweig.
80. Zuk, M., and G. R. Kolluru 1998. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73:415-438.