Evolutionary Ecology

, Volume 25, Issue 2, pp 307–329 | Cite as

Testing the fisherian mechanism: examining the genetic correlation between male song and female response in waxmoths

  • Yihong Zhou
  • John K. Kelly
  • Michael D. Greenfield
Original Paper

Abstract

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to either non-random mate choice or physical linkage. Such linkage disequilibria, a genetic correlation, can accelerate the evolution of male traits and female preferences to exaggerated levels. But relatively few empirical studies have measured the genetic correlation between male traits and female responses in natural populations, and the findings of those few are mixed: often, genetic correlations are not found. We tested the above prediction in an acoustic pyralid moth, Achroia grisella, in which males attract females with a rhythmic train of sound pulses, and females respond only to song that exceeds a minimum pulse rhythm. Both male song rhythm and female threshold response are repeatable and heritable characters. Because female choice in A. grisella is based largely on male song, and males do not appear to provide direct benefits at mating, genetic correlation between male song rhythm and female response is expected. We studied 2 A. grisella populations, bred them according to a full-sib/half-sib design, split the progeny among 4 different environmental conditions, and measured the male song/female response genetic correlation in each of the 8 resulting groups. While song rhythm and response threshold were generally heritable, we found no evidence of significant genetic correlation between these traits. We suggest that the complexity of the various male song characters, of female response to male song, and of correlations between male song characters and between aspects of female response have mitigated the evolution of strong genetic correlation between song and response. Thus, exaggerated levels of trait development may be tempered.

Keywords

Acoustic communication Mate choice Runaway selection Sexual selection Signal evolution 

Notes

Acknowledgments

We thank Bethany Harris, Hannah Hohendorf and Chelsea Medlock (Univ. of Kansas) for assistance in the laboratory and Robin Cargel, Robert Danka (U.S. Dept. Agriculture, Baton Rouge, Louisiana) and Jeffrey Pettis (U.S. Dept. Agriculture, Beltsville, Maryland) for field assistance. Software for analyzing song parameters was developed with the assistance of Simon Gray (Cambridge Electronic Design) and LaRoy Brandt (Univ. Kansas). Critical reviews by Rafael Rodriguez and two anonymous referees greatly improved an earlier version of the manuscript. The project was supported financially by U.S. National Science Foundation grant IOB-0516634.

Supplementary material

10682_2010_9421_MOESM1_ESM.docx (63 kb)
Supplementary material 1 (DOCX 62 kb)

References

  1. Allison JD, Roff DA, Cardé RT (2008) Genetic independence of female signal form and male receiver design in the almond moth, Cadra cautella. J Evol Biol 21:1666–1672CrossRefPubMedGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  4. Bakker TCM (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255–257CrossRefGoogle Scholar
  5. Bakker TCM (1999) The study of intersexual selection using quantitative genetics. Behaviour 136:1237–1266CrossRefGoogle Scholar
  6. Bakker TCM, Pomiankowski A (1995) The genetic basis of female mate preferences. J Evol Biol 8:129–171CrossRefGoogle Scholar
  7. Blows MW (1999) Evolution of the genetic covariance between male and female components of mate recognition: an experimental test. Proc R Soc Lond B 266:2169–2174CrossRefGoogle Scholar
  8. Brandt LSE, Greenfield MD (2004) Condition-dependent traits and the capture of genetic variance in male advertisement song. J Evol Biol 17:821–828CrossRefPubMedGoogle Scholar
  9. Brandt LSE, Ludvar BC, Greenfield MD (2005) Co-occurrence of acceptance thresholds and preference functions in female choice: mate discrimination in the lesser wax moth. Ethology 111:609–625CrossRefGoogle Scholar
  10. Breden F, Hornaday K (1994) Test of indirect models of selection in the Trinidad guppy. Heredity 73:291–297CrossRefGoogle Scholar
  11. Collins RD, Jang Y, Reinhold K, Greenfield MD (1999) Quantitative genetics of ultrasonic advertisement signaling in the lesser waxmoth Achroia grisella (Lepidoptera: Pyralidae). Heredity 83:644–651CrossRefPubMedGoogle Scholar
  12. Danielson-François A, Kelly JK, Greenfield MD (2006) Genotype x environment interaction for male attractiveness in an acoustic moth: evidence for plasticity and canalization. J Evol Biol 19:532–542CrossRefPubMedGoogle Scholar
  13. Danielson-François A, Zhou Y, Greenfield MD (2009) Indirect genetic effects and the lek paradox: inter-genotypic competition may strengthen genotype × environment interactions and conserve genetic variance. Genetica 136:27–36CrossRefPubMedGoogle Scholar
  14. Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New YorkGoogle Scholar
  15. Fry JD (1992) The mixed-model analysis of variance applied to quantitative genetics: biological meaning of the parameters. Evolution 46:540–550CrossRefGoogle Scholar
  16. Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, OxfordGoogle Scholar
  17. Greenfield MD, Baker M (2003) Bat avoidance in non-aerial insects: the silence response of signaling males in an acoustic moth. Ethology 109:427–442CrossRefGoogle Scholar
  18. Greenfield MD, Coffelt JA (1983) Reproductive behaviour of the lesser wax moth, Achroia grisella (Pyralidae: Galleriinae): signalling, pair formation, male interactions, and mate guarding. Behaviour 84:287–315CrossRefGoogle Scholar
  19. Greenfield MD, Medlock C (2007) Temperature coupling as an emergent property: parallel thermal effects on male song and female response do not contribute to species recognition in an acoustic moth. Evolution 61:1590–1599CrossRefPubMedGoogle Scholar
  20. Greenfield MD, Rodriguez RL (2004) Genotype × environment interaction and the reliability of mating signals. Anim Behav 68:1461–1468CrossRefGoogle Scholar
  21. Greenfield MD, Weber T (2000) Evolution of ultrasonic signalling in wax moths: discrimination of ultrasonic mating calls from bat echolocation signals and the exploitation of an anti-predator receiver bias by sexual advertisement. Ethol Ecol Evol 12:259–279CrossRefGoogle Scholar
  22. Greig EI, Greenfield MD (2004) Sexual selection and predator avoidance in an acoustic moth: discriminating females take fewer risks. Behaviour 141:799–815CrossRefGoogle Scholar
  23. Hawthorne DJ, Via S (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904–907CrossRefPubMedGoogle Scholar
  24. Holm S (1979) A simple sequentially-rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  25. Houde AE (1994) Effect of artificial selection on male color patterns on mating preference of female guppies. Proc R Soc Lond B 256:125–130CrossRefGoogle Scholar
  26. Jang Y, Greenfield MD (1996) Ultrasonic communication and sexual selection in wax moths: female choice based on energy and asynchrony of male signals. Anim Behav 51:1095–1106CrossRefGoogle Scholar
  27. Jang Y, Greenfield MD (1998) Absolute versus relative measurements of sexual selection: assessing the contributions of ultrasonic signal characters to mate attraction in lesser wax moths, Achroia grisella (Lepidoptera: Pyralidae). Evolution 52:1383–1393CrossRefGoogle Scholar
  28. Jang Y, Greenfield MD (2000) Quantitative genetics of female choice in an ultrasonic pyralid moth, Achroia grisella: variation and evolvability of preference along multiple dimensions of the male advertisement signal. Heredity 84:73–80CrossRefPubMedGoogle Scholar
  29. Jang Y, Collins RD, Greenfield MD (1997) Variation and repeatability of ultrasonic sexual advertisement signals in Achroia grisella (Lepidoptera: Pyralidae). J Insect Behav 10:87–98CrossRefGoogle Scholar
  30. Kelly JK (2003) Deleterious mutations and the genetic variance of male fitness components in Mimulus guttatus. Genetics 164:1071–1085PubMedGoogle Scholar
  31. Kelly JK, Arathi HS (2003) Inbreeding and the genetic variance in floral traits of Mimulus guttatus. Heredity 90:77–83CrossRefPubMedGoogle Scholar
  32. Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution 36:1–12CrossRefGoogle Scholar
  33. Kirkpatrick M, Hall DW (2004) Sexual selection and sex linkage. Evolution 58:683–691PubMedGoogle Scholar
  34. Künike G (1930) Zur biologie der kleinen wachsmotte, Achroia grisella Fabr. Z Angew Entomol 16:304–356CrossRefGoogle Scholar
  35. Lande R (1981) Models of speciation by sexual selection on polygenic characters. Proc Natl Acad Sci USA 78:3721–3725CrossRefPubMedGoogle Scholar
  36. Löfstedt C, Hansson BS, Roelofs W, Bengtsson BO (1989) No linkage between genes controlling female pheromone production and male pheromone response in the European cornborer, Ostrinia nubilalis Hubner (Lepidoptera: Pyralidae). Genetics 123:553–556PubMedGoogle Scholar
  37. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, SunderlandGoogle Scholar
  38. Milum VG (1940) Moth pests of honey bee combs. Glean Bee Cult 68:424–428Google Scholar
  39. Morris MR, Wagner WE, Ryan MJ (1996) A negative correlation between trait and mate preference in Xiphophorus pygmaeus. Anim Behav 52:1193–1203CrossRefGoogle Scholar
  40. Muhlhauser C, Blanckenhorn WU (2004) The quantitative genetics of sexual selection in the dung fly Sepsis cynipsea. Behaviour 141:327–341CrossRefGoogle Scholar
  41. Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84–86CrossRefPubMedGoogle Scholar
  42. Reeve HK, Pfennig DW (2003) Genetic biases for showy males: are some genetic systems especially conducive to sexual selection? Proc Natl Acad Sci USA 100:1089–1094CrossRefPubMedGoogle Scholar
  43. Ritchie MG, Saarikettu M, Hoikkala A (2005) Variation, but no covariance, in female preference functions and male song in a natural population of Drosophila montana. Anim Behav 70:849–854CrossRefGoogle Scholar
  44. Rodriguez RL, Greenfield MD (2003) Genetic variance and phenotypic plasticity in a component of female mate choice in an ultrasonic moth. Evolution 57:1304–1313PubMedGoogle Scholar
  45. Rodriguez RL, Greenfield MD (2004) Behavioral context regulates dual function of hearing in ultrasonic moths: bat avoidance and pair formation. Physiol Entomol 29:159–168CrossRefGoogle Scholar
  46. Roff DA (1997) Evolutionary quantitative genetics. Chapman & Hall, New YorkGoogle Scholar
  47. Sæther SA, Sætre GP, Borge T, Wiley C, Svedin N, Andersson G, Veen T, Haavie J, Servedio MR, Bureš S, Král M, Hjernquist MB, Gustafsson L, Träff J, Qvarnström A (2007) Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318:95–97CrossRefPubMedGoogle Scholar
  48. Schnitzler HU, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569CrossRefGoogle Scholar
  49. Searle SR, Case A, McCulloch CE (1992) Variance components. Wiley-Interscience, New YorkCrossRefGoogle Scholar
  50. Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93:241–248CrossRefPubMedGoogle Scholar
  51. Shaw RG (1987) Maximum likelihood approaches applied to quantitative genetics of natural populations. Evolution 41:812–826CrossRefGoogle Scholar
  52. Simmons LW, Kotiaho JS (2007) Quantitative genetic correlation between trait and preference supports a sexually selected sperm process. Proc Natl Acad Sci USA 104:16604–16608CrossRefPubMedGoogle Scholar
  53. Spangler HG, Greenfield MD, Takessian A (1984) Ultrasonic mate calling in the lesser wax moth. Physiol Entomol 9:87–95CrossRefGoogle Scholar
  54. Via S (1984) The quantitative genetics of polyphagy in an insect herbivore. I. Genotype-environment interaction in larval performance on different host plant species. Evolution 38:881–895CrossRefGoogle Scholar
  55. Wilkinson GS, Reillo PR (1994) Female choice response to artificial selection on an exaggerated male trait in a stalk-eyed fly. Proc R Soc Lond B 253:1–6CrossRefGoogle Scholar
  56. Zhou Y, Kuster HK, Pettis JS, Danka RG, Gleason JM, Greenfield MD (2008) Reaction norm variants for male calling song in populations of Achroia grisella (Lepidoptera: Pyralidae): towards a resolution of the lek paradox. Evolution 62:1317–1334CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Yihong Zhou
    • 1
    • 2
  • John K. Kelly
    • 1
  • Michael D. Greenfield
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of KansasLawrenceUSA
  2. 2.Department of BiologyUniversity of VermontBurlingtonUSA
  3. 3.Institut de Recherche Sur la Biologie de l’insecte, CNRS UMR 6035Université François Rabelais de ToursToursFrance

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