Evolutionary Ecology

, 22:103

Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs

Original Paper

Abstract

In this study we investigated the developmental basis of adult phenotypes in a non-model organism, a polymorphic damselfly (Ischnura elegans) with three female colour morphs. This polymorphic species presents an ideal opportunity to study intraspecific variation in growth trajectories, morphological variation in size and shape during the course of ontogeny, and to relate these juvenile differences to the phenotypic differences of the discrete adult phenotypes; the two sexes and the three female morphs. We raised larvae of different families in individual enclosures in the laboratory, and traced morphological changes during the course of ontogeny. We used principal components analysis to examine the effects of Sex, Maternal morph, and Own morph on body size and body shape. We also investigated the larval fitness consequences of variation in size and shape by relating these factors to emergence success. Females grew faster than males and were larger as adults, and there was sexual dimorphism in body shape in both larval and adult stages. There were also significant effects of both maternal morph and own morph on growth rate and body shape in the larval stage. There were significant differences in body shape, but not body size, between the adult female morphs, indicating phenotypic integration between colour, melanin patterning, and body shape. Individuals that emerged successfully grew faster and had different body shape in the larval stage, indicating internal (non-ecological) selection on larval morphology. Overall, morphological differences between individuals at the larval stage carried over to the adult stage. Thus, selection in the larval stage can potentially result in correlated responses in adult phenotypes and vice versa.

Keywords

Alternative phenotypes Antagonistic selection Complex life-cycle Correlational selection Mimicry Sexual conflict 

References

  1. Abbott JK (2006) Ontogeny and population biology of a sex-limited colour polymorphism (PhD thesis). Lund University, Lund, SwedenGoogle Scholar
  2. Abbott J, Svensson EI (2005) Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly. J Evol Biol 18:1464–1470PubMedGoogle Scholar
  3. Arthur W (2002) The emerging conceptual framework of evolutionary developmental biology. Nature 415:757–764PubMedGoogle Scholar
  4. Askew RR (1988) The dragonflies of Europe. Harley Books, Colchester, EssexGoogle Scholar
  5. Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17:369–378CrossRefGoogle Scholar
  6. Badyaev AV (2004) Developmental perspective on the evolution of sexual ornaments. Evol Ecol Res 6:975–991Google Scholar
  7. Badyaev AV, Hill GE, Dunn PO, Glen JC (2001a) Plumage color as a composite trait: developmental and functional integration of sexual ornamentation. Am Nat 158:221–235CrossRefGoogle Scholar
  8. Badyaev AV, Whittingham LA, Hill GE (2001b) The evolution of sexual size dimorphism in the house finch. III. Developmental basis. Evolution 55:176–189Google Scholar
  9. Banks MJ, Thompson DJ (1987) Regulation of damselfly populations: the effects of larval density on larval survival, development rate and size in the field. Freshwater Biol 17:357–365CrossRefGoogle Scholar
  10. Benke AC (1970) A method for comparing individual growth rates of aquatic insects with special reference to the Odonata. Ecology 51:328–331CrossRefGoogle Scholar
  11. Bolnick DI, Doebeli M (2003) Sexual dimorphism and adaptive speciation: two sides of the same ecological coin. Evolution 57:2433–2449PubMedGoogle Scholar
  12. Borash DJ, Gibbs AG, Joshi A, Mueller LD (1998) A genetic polymorphism maintained by natural selection in a temporally varying environment. Am Nat 151:148–156CrossRefPubMedGoogle Scholar
  13. Brodie ED III (1992) Correlational selection for colour pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–1298CrossRefGoogle Scholar
  14. Carchini G, Chiarotti F, Di Domenico M, Paganotti G (2000) Fluctuating asymmetry, size and mating success in males of Ischnura elegans (Vander Linden) (Odonata: Coenagrionidae). Anim Behav 59:177–182PubMedCrossRefGoogle Scholar
  15. Cooper G, Miller PL, Holland PWH (1996) Molecular genetic analysis of sperm competition in the damselfly Ischnura elegans (Vander Linden). Proc R Soc Lond B Biol Sci 263:1343–1349CrossRefGoogle Scholar
  16. Corbet PS (1999) Dragonflies: behaviour and ecology of Odonata. Harley Books, Colchester, EssexGoogle Scholar
  17. Cordero A (1990) The inheritance of female polymorphism in the damselfly Ischnura graellsii (Rambur) (Odonata: Coenagrionidae). Heredity 64:341–346Google Scholar
  18. Cordero A (1991) Fecundity of Ischnura graellsii (Rambur) in the laboratory (Zygoptera: Coenagrionidae). Odonatologica 20:37–44Google Scholar
  19. Cordero A (1992a) Density-dependent mating success and colour polymorphism in females of the damselfly Ischnura graellsii (Odonata: Coenagrionidae). J Anim Ecol 61:769–780CrossRefGoogle Scholar
  20. Cordero A (1992b) Morphological variability, female polymorphism and heritability of body length in Ischnura graellsii (Rambur) (Zygoptera: Coenagrionidae). Odonatologica 21:409–419Google Scholar
  21. Cordero A, Santolamazza Carbone S, Utzeri C (1997) Male mating success in a natural population of Ischnura elegans (Vander Linden) (Odonata: Coenagrionidae). Odonatologica 26:459–465Google Scholar
  22. Cordero A, Santolamazza Carbone S, Utzeri C (1998) Mating opportunities and mating costs are reduced in androchrome female damselflies, Ischnura elegans (Odonata). Anim. Behav. 55:185–197PubMedCrossRefGoogle Scholar
  23. de Block M, Stoks R (2003) Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly. J Evol Biol 16:986–995PubMedCrossRefGoogle Scholar
  24. Fincke OM (2004) Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 67:833–845CrossRefGoogle Scholar
  25. Fry JD (1992) The mixed-model analysis of variance applied to quantitative genetics: biological meaning of the parameters. Evolution 46:540–550CrossRefGoogle Scholar
  26. Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Nat Acad Sci USA 99:10533–10538PubMedCrossRefGoogle Scholar
  27. Gilbert SF (2001) Ecological developmental biology: developmental biology meets the real world. Dev Biol 233:1–12PubMedCrossRefGoogle Scholar
  28. Harvey IF, Corbet PS (1985) Territorial behaviour of larvae enhances mating success of male dragonflies. Anim Behav 33:561–565CrossRefGoogle Scholar
  29. Jackson JE (1991) A user’s guide to principal components. John Wiley & Sons, Inc., New YorkGoogle Scholar
  30. Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope’s Rule of phyletic size increase. Evolution 58:1608–1612PubMedGoogle Scholar
  31. Leimar O (2005) The evolution of phenotypic polymorphism: randomized strategies versus evolutionary branching. Am Nat 165:669–681PubMedCrossRefGoogle Scholar
  32. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996). SAS system for mixed models. SAS Institute Inc., Cary, NCGoogle Scholar
  33. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc., Sunderland, MAGoogle Scholar
  34. McGlothlin JW, Parker PG, Nolan V Jr, Ketterson ED (2005) Correlational selection leads to genetic integration of body size and an attractive plumage trait in Dark-eyed Juncos. Evolution 59:658–671PubMedGoogle Scholar
  35. Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding ares: a review. Ecol Lett 4:663–673CrossRefGoogle Scholar
  36. Mueller LD (1988) Evolution of competitive ability in Drosophila by density-dependent natural selection. Proc Nat Acad Sci USA 85:4383–4386PubMedCrossRefGoogle Scholar
  37. Mueller LD, Ayala FJ (1981). Trade-off between r-selection and K-selection in Drosophila populations. Proc Nat Acad Sci USA 78:1303–1305PubMedCrossRefGoogle Scholar
  38. Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett 6:265–272CrossRefGoogle Scholar
  39. Pigliucci M, Preston K (eds) (2004) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, OxfordGoogle Scholar
  40. Rice WR, Chippindale AK (2001) Intersexual ontogenetic conflict. J Evol Biol 14:685–693CrossRefGoogle Scholar
  41. Rose MR (1982) Antagonistic pleiotropy, dominance and genetic variation. Heredity 48:63–78Google Scholar
  42. Sánchez-Guillén RA, Van Gossum H, Cordero Rivera A (2005) Hybridization and the inheritance of female colour polymorphism in two Ischnurid damselflies (Odonata: Coenagrionidae). Biol J Linn Soc 85:471–481CrossRefGoogle Scholar
  43. Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774CrossRefGoogle Scholar
  44. Schwenk K, Wagner GP (2001) Function and the evolution of phenotypic stability: connecting pattern to process. Am Zool 41:552–563CrossRefGoogle Scholar
  45. Shuster SM, Sassaman C (1997) Genetic interaction between male mating strategy and sex ration in a marine isopod. Nature 388:373–377CrossRefGoogle Scholar
  46. Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380:240–243CrossRefGoogle Scholar
  47. Sinervo B, Svensson E (2002) Correlational selection and the evolution of genomic architecture. Heredity 89:329–338PubMedCrossRefGoogle Scholar
  48. Sinervo B, Svensson E, Comendant T (2000) Density cycles and an offspring quantity and quality game driven by natural selection. Nature 406:985–988PubMedCrossRefGoogle Scholar
  49. Sirot LK, Brockmann HJ (2001) Costs of sexual interactions to females in Rambur’s forktail damselfly, Ischnura ramburi (Zygoptera: Coenagrionidae). Anim Behav 61:415–424CrossRefGoogle Scholar
  50. Stoks R., McPeek MA, Mitchell JL (2003) Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes. Evolution 57:574–585PubMedGoogle Scholar
  51. Stoks R, Nystrom JL, May ML, McPeek MA (2005) Parallel evolution in ecological and reproductive traits to produce cryptic damselfly species across the holarctic. Evolution 59:1976–1988PubMedGoogle Scholar
  52. Svensson E, Sinervo B, Comendant T (2001) Condition, genotype-by-environment interaction, and correlational selection in lizard life-history morphs. Evolution 55:2053–2069PubMedGoogle Scholar
  53. Svensson EI, Abbott J (2005) Evolutionary dynamics and population biology of a polymorphic insect. J Evol Biol 18:1503–1514PubMedCrossRefGoogle Scholar
  54. Svensson EI, Abbott J, Härdling R (2005) Female polymorphism, frequency-dependence and rapid evolutionary dynamics in natural populations. Am Nat 165:567–576PubMedCrossRefGoogle Scholar
  55. Van Gossum H, Stoks R, De Bruyn L (2001) Frequency-dependent male mate harassment and intra-specific variation in its avoidance by females of the damselfly. Ischnura elegans. Behav Ecol Sociobiol 51:69–75CrossRefGoogle Scholar
  56. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  1. 1.Section for Animal EcologyLund UniversityLundSweden

Personalised recommendations