Evaluating female remating rates in light of spermatophore degradation in Heliconius butterflies: Pupal-mating monandry versus adult-mating polyandry

Ecological Entomology

Volumn 37, Issue 4, 2012, Pages 257-268

  Walters, James R ^a,b   Corbins, Chris ^a   Hardcastle, Thomas J ^a   Jiggins, Chris D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Lepidoptera; Mating systems; Sexual selection; Spermatophore counts

Indexed keywords

ADULT; BUTTERFLY; CAPTIVE BREEDING; COMPARATIVE STUDY; FEMALE; POLYANDRY; PUPA; REPRODUCTIVE STRATEGY; SEXUAL SELECTION; SPERMATOPHORE;

HELICONIUS; HELICONIUS ERATO; LEPIDOPTERA; PAPILIONOIDEA;

EID: 84863767449     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2012.01360.x     Document Type: Article

References (43)

1. Arnqvist, G. & Nilsson, T. (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour, 60, 145-164.
2. Arnqvist, G., Edvardsson, M., Friberg, U. & Nilsson, T. (2000) Sexual conflict promotes speciation in insects. Proceedings of the National Academy of Sciences of the United States of America, 97, 10460-10464.
3. Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity, 2, 349-368.
4. Beltran, M., Jiggins, C.D., Brower, A.V.Z., Bermingham, E. & Mallet, J. (2007) Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biological journal of the Linnean Society, 92, 221-239.
5. Boggs, C.L. (1979) Resource allocation and reproductive strategies in several Heliconiine butterfly species. PhD thesis, Unviersity of Texas, Austin.
6. Boggs, C. (1981) Selection pressures affecting male nutrient investment at mating in Heliconiine butterflies. Evolution, 35, 931-940.
7. Boggs, C. (1990) A general-model of the role of male-donated nutrients in female insects reproduction. The American Naturalist, 136, 598-617.
8. Boggs, C.L. & Gilbert, L.E. (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science, 206, 83-84.
9. Boyko, A.R. (2005) The evolution of warning coloration in Heliconius butterflies. PhD thesis, Purdue University, West Lafayette, Indiana.
10. Brown, K.S. (1981) The biology of Heliconius and related genera. Annual Review of Entomology, 26, 427-456.
11. Bundgaard, J., Barker, J.S.F., Frydenberg, J. & Clark, A.G. (2004) Remating and sperm displacement in a natural population of Drosophila buzzatii inferred from mother-offspring analysis of microsatellite loci. Journal of Evolutionary Biology, 17, 376-381.
12. Burns, J.M. (1968) Mating frequency in natural population of skippers and butterflies as determined by spermatophore counts. Proceedings of the National Academy of Sciences of the United States of America, 61, 852-859.
13. Cardoso, M.Z., Roper, J.J. & Gilbert, L.E. (2009) Prenuptial agreements: mating frequency predicts gift-giving in Heliconius species. Entomologia Experimentalis et Applicata, 131, 109-114.
14. Cook, L.M., Thomason, E.W. & Young, A.M. (1976) Population structure, dynamics and dispersal of the tropical butterfly Heliconius charitonius. Journal of Animal Ecology, 45, 851-863.
15. Deinert, E.L. (2003) Mate location and competition for mates in a pupal mating butterfly. Butterflies: Ecology and Evolution Taking Flight (ed. by C. L. Boggs, W. B. Watt and P. Ehrlich ), pp. 91-108. University of Chicago Press, Chicago, Illinois.
16. Deinert, E., Longino, J. & Gilbert, L. (1994) Mate competition in butterflies. Nature, 370, 23-24.
17. Drummond, B.A. (1984) Multiple mating and sperm competition in the Lepidoptera. Sperm Competition and the Evolution of Animal Mating Systems (ed. by R. L. Smith ), pp. 291-370. Academic press, New York, New York.
18. Ehrlich, A.H. & Ehrlich, P.R. (1978) Reproductive strategies in the butterflies: I. Mating frequency, plugging, and egg number. Journal of the Kansas Entomological Society, 51, 666-697.
19. Estrada, C., Schulz, S., Yildizhan, S. & Gilbert, L.E. (2011) Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies. Evolution, 65, 2843-2854.
20. Gilbert, L.E. (1976) Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? Science, 193, 419-420.
21. Gillott, C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology, 48, 163-184.
22. González, A., Rossini, C., Eisner, M. & Eisner, T. (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proceedings of the National Academy of Sciences of the United States of America, 96, 5570-5574.
23. Hosken, D.J., Stockley, P., Tregenza, T. & Wedell, N. (2009) Monogamy and the battle of the sexes. Annual Review of Entomology, 54, 361-378.
24. Huignard, J. (1983) Transfer and fate of male secretions deposited in the spermatophore of females of acanthoscelides-obtectus say (Coleoptera, Bruchidae). Journal of Insect Physiology, 29, 55-53.
25. Kuijper, B. & Morrow, E.H. (2009) Direct observation of female mating frequency using time-lapse photography. Fly, 3, 118-120.
26. Mann, T. (1984) Spermatophores: Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa (Zoophysiology). Springer, New York, New York.
27. Penz, C. (1999) Higher level phylogeny for the passion-vine butterflies (Nymphalidae, Heliconiinae) based on early stage and adult morphology. Journal of the Linnean Society of London, 127, 277-344.
28. Pliske, T.E. (1973) Factors determining mating frequencies in some new world butterflies and skippers. Annals of the Entomological Society of America, 66, 164-169.
29. Price, T.A.R., Lewis, Z., Smith, D.T., Hurst, G.D.D. & Wedell, N. (2011) Remating in the laboratory reflects rates of polyandry in the wild. Animal Behaviour, 82, 1381-1386.
30. Quintero, H. (1988) Population dynamics of the butterfly Heliconius charitonius L. in Puerto Rico. Caribbean Journal of Science, 24, 155-160.
31. R Development Core Team (2011) R: A language and environment for statistical computing.
32. van der Reijden, E., Monchamp, J. & Lewis, S. (1997) The formation, transfer, and fate of spermatophores in Photinus fireflies (Coleoptera:Lampyridae). Canadian Journal of Zoology, 75, 1202-1207.
33. Reinhardt, K., Koehler, G., Webb, S. & Childs, D. (2007) Field mating rate of female meadow grasshoppers, Chorthippus parallelus, estimated from sperm counts. Ecological Entomology, 32, 637-642.
34. Rhainds, M. (2010) Female mating failures in insects. Entomologia Experimentalis et Applicata, 136, 211-226.
35. Rodriguez-Munoz, R., Bretman, A., Slate, J., Walling, C.A. & Tregenza, T. (2010) Natural and sexual selection in a wild insect population. Science, 328, 1269-1272.
36. Sánchez, V., Hernández-Baños, B.E. & Cordero, C. (2011) The evolution of a female genital trait widely distributed in the Lepidoptera: comparative evidence for an effect of sexual coevolution. PLoS ONE, 6, e22642.
37. Schulz, S., Estrada, C., Yildizhan, S., Boppré, M. & Gilbert, L.E. (2008) An antiaphrodisiac in Heliconius melpomene butterflies. Journal of Chemical Ecology, 34, 82-93.
38. Scott, J.A. (1972) Mating of butterflies. Journal of Research on the Lepidoptera, 11, 99-127.
39. Simmons, L.W. (2001) Sperm Competition and Its Evolutionary Consequences in the Insects. Princeton University Press, Princeton, New Jersey.
40. Vahed, K. (1998) The function of nuptial feeding in insects: review of empirical studies. Biological Reviews, 73, 43-78.
41. Walters, J.R. & Harrison, R.G. (2011) Decoupling of rapid and adaptive evolution among seminal fluid proteins in heliconius butterflies with divergent mating systems. Evolution, 65, 2855-2871.
42. Wedell, N., Wiklund, C. & Cook, P. (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behavioral Ecology, 13, 450-455.
43. Wigby, S. & Chapman, T. (2005) Sex peptide causes mating costs in female Drosophila melanogaster. Current Biology, 15, 316-321.