Evolutionary Ecology

, Volume 24, Issue 1, pp 83–95 | Cite as

Eyespan reflects reproductive quality in wild stalk-eyed flies

  • Samuel CottonEmail author
  • Jennifer Small
  • Rosli Hashim
  • Andrew Pomiankowski
Original Paper


Handicap models of sexual selection propose that females use male sexual ornaments as a cue in mate choice because they reflect commodities that increase female fitness, either directly or indirectly. In contrast to studies on vertebrates, most investigations of ornaments in insects and other invertebrate taxa have been conducted under laboratory conditions. There is a pressing need to address questions relating to sexual signalling of quality in natural populations, as the arbitrary and uniform environments found in the laboratory fail to reflect the world under which animals have evolved. We investigated associations between male ornaments (exaggerated eyespan), attractiveness, and reproductive quality in a wild population of the sexually ornamented stalk-eyed fly, Teleopsis dalmanni. We also explored the relationship between eyespan and reproductive quality in females to evaluate the potential for sexually antagonistic selection on eyespan. We show that eyespan is a generic correlate of reproductive quality, acting as a reliable mirror of variation in reproductive fitness in both sexes. Our findings suggest that male ornaments signal commodities that are of interest to females in the natural environment in which they, and mate preferences for them, have evolved. In addition, the covariance between female eyespan and reproductive output suggests that the former may be a reliable cue of quality in its own right. Our data provide important insights into the evolutionary forces that shape the evolution of exaggerated eyespan in wild populations of this species.


Sexual selection Ornaments Wild Stalk-eyed fly Testis Accessory glands Fecundity Fertility 



This work was supported by awards from the Association for the Study of Animal Behaviour (A.P. and R.H.), the Royal Society (A.P. and R.H.), the BBSRC (grants to K. Fowler, A.P., T. Chapman and H. Smith; studentship to J.S.), the Department of Biology, University College London (J.S. and A.P.), and a NERC Fellowship (S.C.). We thank two anonymous reviewers for comments on a previous version of the manuscript, and staff at the Gombak Valley Field Research Centre, University of Malaya, Kuala Lumpur for assistance.


  1. Al-khairulla H, Warburton D, Knell RJ (2003) Do the eyestalks of female Diopsid flies have a function in intrasexual aggressive encounters? J Insect Behav 16:679–686. doi: 10.1023/ CrossRefGoogle Scholar
  2. Andersson M (1986) Evolution of condition-dependent sex ornaments and mating preferences; sexual selection based on viability differences. Evol Int J Org Evol 40:804–816. doi: 10.2307/2408465 Google Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Baker RH, Wilkinson GS (2001) Phylogenetic analysis of sexual dimorphism and eyespan allometry in stalk-eyed flies (Diopsidae). Evol Int J Org Evol 55:1373–1385Google Scholar
  5. Baker RH, Ashwell RIS, Richards TA et al (2001) Effects of multiple mating and male eye span on female reproductive output in the stalk-eyed fly Cyrtodiopsis dalmanni. Behav Ecol 12:732–739. doi: 10.1093/beheco/12.6.732 CrossRefGoogle Scholar
  6. Baker RH, Denniff M, Futerman P et al (2003) Accessory gland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav Ecol 14:607–611. doi: 10.1093/beheco/arg053 CrossRefGoogle Scholar
  7. Bjorksten TA, Pomiankowski A, Fowler K (2001) Temperature shock during development fails to increase the fluctuating asymmetry of a sexual trait in stalk-eyed flies. Proc R Soc Lond B Biol Sci 268:1503–1510. doi: 10.1098/rspb.2001.1575 CrossRefGoogle Scholar
  8. Burkhardt D, de la Motte I (1985) Selective pressures, variability, and sexual dimorphism in stalk-eyed flies (Diopsidae). Naturwissenschaften 72:204–206. doi: 10.1007/BF01195763 CrossRefGoogle Scholar
  9. Charmantier A, Sheldon BC (2006) Testing genetic models of mate choice evolution in the wild. Trends Ecol Evol 21:417–419. doi: 10.1016/j.tree.2006.06.001 CrossRefPubMedGoogle Scholar
  10. Cornwallis CK, Birkhead TR (2008) Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits. Evol Int J Org Evol 62:1149–1161. doi: 10.1111/j.1558-5646.2008.00346.x Google Scholar
  11. Cotton S, Fowler K, Pomiankowski A (2004a) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B Biol Sci 271:771–783. doi: 10.1098/rspb.2004.2688 CrossRefGoogle Scholar
  12. Cotton S, Fowler K, Pomiankowski A (2004b) Condition dependence of sexual ornament size and variation in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera: Diopsidae). Evol Int J Org Evol 58:1038–1046Google Scholar
  13. Cotton S, Fowler K, Pomiankowski A (2004c) Heightened condition dependence is not a general feature of male eyespan in stalk-eyed flies (Diptera: Diopsidae). J Evol Biol 17:1310–1316. doi: 10.1111/j.1420-9101.2004.00754.x CrossRefPubMedGoogle Scholar
  14. David P, Hingle A, Greig D et al (1998) Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies. Proc R Soc Lond B Biol Sci 265:2211–2216. doi: 10.1098/rspb.1998.0561 CrossRefGoogle Scholar
  15. David P, Bjorksten T, Fowler K et al (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188. doi: 10.1038/35018079 CrossRefPubMedGoogle Scholar
  16. Ellegren H, Sheldon BS (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175. doi: 10.1038/nature06737 CrossRefPubMedGoogle Scholar
  17. Fisher RA (1958) The genetical theory of natural selection. Clarendon Press, Oxford (reprinted 1999, Oxford Univ Press, Oxford)Google Scholar
  18. Fry C (2006) Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol Dev 8:191–201. doi: 10.1111/j.1525-142X.2006.00089.x CrossRefPubMedGoogle Scholar
  19. Getty T (2006) Sexually selected signals are not similar to sports handicaps. Trends Ecol Evol 21:83–88. doi: 10.1016/j.tree.2005.10.016 CrossRefPubMedGoogle Scholar
  20. Grafen A (1990) Sexual selection unhandicapped by the fisher process. J Theor Biol 144:473–516. doi: 10.1016/S0022-5193(05)80087-6 CrossRefPubMedGoogle Scholar
  21. Greenfield MD (1997) Sexual selection in resource defense polygamy: lessons from territorial grasshoppers. In: Chloe J, Crespi B (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 75–88Google Scholar
  22. Hingle A, Fowler K, Pomiankowski A (2001a) Size-dependent mate preference in the stalk-eyed fly Cyrtodiopsis dalmanni. Anim Behav 61:589–595. doi: 10.1006/anbe.2000.1613 CrossRefGoogle Scholar
  23. Hingle A, Fowler K, Pomiankowski A (2001b) The effect of transient food stress on female mate preference in the stalk-eyed fly Cyrtodiopsis dalmanni. Proc R Soc Lond B Biol Sci 268:1239–1244. doi: 10.1098/rspb.2001.1647 CrossRefGoogle Scholar
  24. Iwasa Y, Pomiankowski A (1994) The evolution of mate preferences for multiple handicaps. Evol Int J Org Evol 48:853–867. doi: 10.2307/2410492 Google Scholar
  25. Iwasa Y, Pomiankowski A (1999) Good parent and good genes models of handicap evolution. J Theor Biol 200:97–109. doi: 10.1006/jtbi.1999.0979 CrossRefPubMedGoogle Scholar
  26. Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences. II. The “handicap” principle. Evol Int J Org Evol 45:1431–1442. doi: 10.2307/2409890 Google Scholar
  27. Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev Camb Philos Soc 70:1–65. doi: 10.1111/j.1469-185X.1995.tb01439.x CrossRefPubMedGoogle Scholar
  28. King RC (1970) Ovarian development in Drosophila melanogaster. Academic Press, New YorkGoogle Scholar
  29. Kokko H, Jennions MD, Brooks R (2006) Unifying and testing models of sexual selection. Annu Rev Ecol Syst 37:43–66. doi: 10.1146/annurev.ecolsys.37.091305.110259 CrossRefGoogle Scholar
  30. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evol Int J Org Evol 34:292–305. doi: 10.2307/2407393 Google Scholar
  31. Lande R, Arnold SJ (1985) Evolution of mating preference and sexual dimorphism. J Theor Biol 117:651–664. doi: 10.1016/S0022-5193(85)80245-9 CrossRefPubMedGoogle Scholar
  32. Lorch P, Wilkinson GS, Reillo RP (1993) Copulation duration and sperm precedence in the stalk-eyed fly Cyrtodiopsis whitei. Behav Ecol Sociobiol 32:303–311. doi: 10.1007/BF00183785 CrossRefGoogle Scholar
  33. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  34. Meier R, Baker RH (2002) A cladistic analysis of Diopsidae (Diptera) based on morphological and DNA sequence data. Insect Syst Evol 33:325–336CrossRefGoogle Scholar
  35. Panhuis TM, Wilkinson GS (1999) Exaggerated eyespan influences male contest outcome in stalk-eyed flies. Behav Ecol Sociobiol 46:221–227. doi: 10.1007/s002650050613 CrossRefGoogle Scholar
  36. Pomiankowski A (1987) Sexual selection: the handicap principle does work—sometimes. Proc R Soc Lond B Biol Sci 231:123–145CrossRefGoogle Scholar
  37. Pomiankowski A (1988) The evolution of female mate preferences for male genetic quality. Ox Surv Evol Biol 5:136–184Google Scholar
  38. Rogers DW, Baker RH, Chapman T et al (2005a) Direct and correlated responses to artificial selection on male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni. J Evol Biol 18:642–650. doi: 10.1111/j.1420-9101.2004.00860.x CrossRefPubMedGoogle Scholar
  39. Rogers DW, Chapman T, Fowler K et al (2005b) Mating-induced reduction in reproductive organ size in the stalk-eyed fly Cyrtodiopsis dalmanni. BMC Evol Biol 5:37. doi: 10.1186/1471-2148-5-37 CrossRefPubMedGoogle Scholar
  40. Rogers DW, Grant CA, Chapman T et al (2006) The influence of male and female eyespan on fertility in the stalk-eyed fly Cyrtodiopsis dalmanni. Anim Behav 72:1363–1369. doi: 10.1016/j.anbehav.2006.03.027 CrossRefGoogle Scholar
  41. Rogers DW, Denniff M, Chapman T et al (2008) Male ornament size signals reproductive quality in the stalk-eyed fly Teleopsis dalmanni. BMC Evol Biol 8:236CrossRefGoogle Scholar
  42. Sgrò CM, Hoffmann AA (2004) Genetic correlations, trade-offs and environmental variation. Heredity 93:241–248. doi: 10.1038/sj.hdy.6800532 CrossRefPubMedGoogle Scholar
  43. Simmons LW, Emlen DJ (2006) Evolutionary trade-off between weapons and testes. Proc Natl Acad Sci USA 103:16346–16351. doi: 10.1073/pnas.0603474103 CrossRefPubMedGoogle Scholar
  44. Simmons LW, Zuk M, Rotenberry JT (2005) Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus. Anim Behav 69:1235–1241. doi: 10.1016/j.anbehav.2004.09.011 CrossRefGoogle Scholar
  45. Wilkinson GS (1993) Artificial selection alters allometry in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera: Diopsidae). Genet Res Camb 62:213–222CrossRefGoogle Scholar
  46. Wilkinson GS, Dodson GN (1997) Function and evolution of antlers and eye stalks in flies. In: Chloe J, Crespi B (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 310–328Google Scholar
  47. Wilkinson GS, Reillo PR (1994) Female choice response to artificial selection in an exaggerated male trait in a stalk-eyed fly. Proc R Soc Lond B Biol Sci 225:1–6. doi: 10.1098/rspb.1994.0001 CrossRefGoogle Scholar
  48. Wilkinson GS, Amitin EG, Johns PM (2005) Sex-linked correlated responses in female reproductive traits to selection on male eye span in stalk-eyed flies. Integr Comp Biol 45:500–510. doi: 10.1093/icb/45.3.500 CrossRefGoogle Scholar
  49. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214. doi: 10.1016/0022-5193(75)90111-3 CrossRefPubMedGoogle Scholar
  50. Zuk M (1988) Parasite load, body size, and age of wild-caught male field crickets (Orthoptera: Gryllidae): effects on sexual selection. Evol Int J Org Evol 42:969–976. doi: 10.2307/2408912 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Samuel Cotton
    • 1
    Email author
  • Jennifer Small
    • 1
  • Rosli Hashim
    • 2
  • Andrew Pomiankowski
    • 1
    • 3
  1. 1.Research Department of Genetics, Evolution and EnvironmentUniversity College LondonLondonUK
  2. 2.Institute of Biological ScienceUniversity of MalayaKuala LumpurMalaysia
  3. 3.CoMPLEXUniversity College LondonLondonUK

Personalised recommendations