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Evolutionary Ecology

, Volume 25, Issue 4, pp 857–873 | Cite as

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

  • Isabel M. SmallegangeEmail author
Research Article

Abstract

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.

Keywords

Differential allocation hypothesis Environmentally cued threshold model Liability Life-history trade-offs Male attractiveness Reaction norm between age and size at maturity 

Notes

Acknowledgments

I thank Tim Coulson and Mark Roberts for discussion and comments, and The Netherlands Organisation for Scientific Research for funding (Rubicon Fellowship). All experimental work conducted in this study conforms to the legal requirements of the UK.

Supplementary material

10682_2010_9446_MOESM1_ESM.doc (64 kb)
Supplementary material 1 (DOC 65 kb)

References

  1. Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412CrossRefGoogle Scholar
  2. Bashey F (2006) Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata. Ecology 60:348–361Google Scholar
  3. Bates D, Sarkar D (2007) lme4: linear mixed-effects models using S4 classes. R package version 0.9975-13Google Scholar
  4. Benton TG, Plaistow SJ, Beckerman AP et al (2005) Changes in maternal investment in eggs can affect population dynamics. Proc R Soc Lond B 272:1351–1356CrossRefGoogle Scholar
  5. Brockmann HJ, Taborsky M (2008) Alternative reproductive tactics and the evolution of alternative allocation phenotypes. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics. Cambridge University Press, Cambridge, pp 25–51CrossRefGoogle Scholar
  6. Brockmann HJ, Oliveira RF, Taborsky M (2008) In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics. Cambridge University Press, Cambridge, pp 471–489Google Scholar
  7. Brody MS, Lawlor LR (1984) Adaptive variation in offspring size in the terrestrial isopod, Armadillidium vulgare. Oecologia 61:55–59CrossRefGoogle Scholar
  8. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445CrossRefGoogle Scholar
  9. Cohen J (1988) Statistical power analysis for the behavioral sciences. Erlbaum, HillsdaleGoogle Scholar
  10. Coulson T, Tuljapurkar S, Childs DZ (2010) Using evolutionary demography to link life history theory, quantitative genetics and population ecology. J Anim Ecol 79:1226–1240PubMedCrossRefGoogle Scholar
  11. Cunningham EJ, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedCrossRefGoogle Scholar
  12. Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350PubMedCrossRefGoogle Scholar
  13. Eberhard WG, Gutiérrez EE (1991) Male dimorphisms in beetles and earwigs and the question of developmental constraints. Evolution 45:18–28CrossRefGoogle Scholar
  14. Emlen DJ (1994) Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera, Scarabaeidae). Proc R Soc Lond B 256:131–136CrossRefGoogle Scholar
  15. Emlen DJ (2008) The roles of genes and the environment in the expression and evolution of alternative tactics. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics. Cambridge University Press, Cambridge, pp 83–108Google Scholar
  16. Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Wiley, New YorkGoogle Scholar
  17. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Pearson Education Ltd, HarlowGoogle Scholar
  18. Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369PubMedCrossRefGoogle Scholar
  19. Fox CW, Thakar MS, Mousseau TA (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat 149:149–163CrossRefGoogle Scholar
  20. Gerson U, Capua S, Thorens D (1983) Life history and life tables of Rhizoglyphus robini Claparède (Acari: Astigmata: Acaridae). Acarologia 24:439–448Google Scholar
  21. Gerson U, Cohen E, Capua S (1991) Bulb mite, Rhizglyphus robini (Astigmata: Acaridae) as an experimental animal. Exp Appl Acarol 12:103–110CrossRefGoogle Scholar
  22. Gil D, Graves J, Hazon N et al (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  23. Hazel WN, Smock R, Johnson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc R Soc Lond B 242:181–187CrossRefGoogle Scholar
  24. Hazel WN, Smock R, Lively CM (2004) The ecological genetics of conditional strategies. Am Nat 163:888–900PubMedCrossRefGoogle Scholar
  25. Hunt J, Simmons LW (2000) Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus. Evolution 54:936–941PubMedGoogle Scholar
  26. Hunt J, Simmons LW (2001) Status-dependent selection in the dimorphic beetle Onthophagus taurus. Proc R Soc Lond B 268:2409–2414CrossRefGoogle Scholar
  27. Kirkpatrick LM, Lande R (1989) The evolution of maternal characters. Evolution 43:485–503CrossRefGoogle Scholar
  28. Kolm N (2001) Females produce larger eggs for large males in a paternal mouthbrooding fish. Proc R Soc Lond B 268:2229–2234CrossRefGoogle Scholar
  29. Kotiaho JS, Simmons LW, Hunt J et al (2003) Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus. Am Nat 161:852–859PubMedCrossRefGoogle Scholar
  30. Kruuk LEB (2004) Estimating genetic parameters in wild populations using the ‘animal model’. Philos Trans R Soc Lond B 359:873–890CrossRefGoogle Scholar
  31. Michimae H, Nishimura K, Tamori Y, Wakahara M (2009) Maternal effects on phenotypic plasticity in larvae of the salamander Hynobius retardatus. Oecologia 160:601–608PubMedCrossRefGoogle Scholar
  32. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, OxfordGoogle Scholar
  33. Oliveira RF, Taborsky M, Brockmann HJ (eds) (2008) Alternative reproductive tactics. Cambridge University Press, CambridgeGoogle Scholar
  34. Plummer M, Best N, Cowles K et al. (2006) Coda: output analysis and diagnostics for MCMC. R package version 0.10-7Google Scholar
  35. Radwan J (1993) The adaptive significance of male polymorphism in the acarid mite Caloglyphus berlesei. Behav Ecol Sociobiol 33:201–208CrossRefGoogle Scholar
  36. Radwan J (1995) Male morph determination in 2 species of acarid mites. Heredity 74:669–673CrossRefGoogle Scholar
  37. Radwan J (2001) Male morph determination in Rhizoglyphus echinopus. Exp Appl Acarol 25:143–149PubMedCrossRefGoogle Scholar
  38. Radwan J (2003) Heritability of male morph in the bulb mite, Rhizoglyphus robini (Astigmata, Acaridae). Exp Appl Acarol 29:109–114PubMedCrossRefGoogle Scholar
  39. Radwan J (2009) Alternative mating tactics in acarid mites. Adv Stud Behav 39:185–208CrossRefGoogle Scholar
  40. Radwan J, Klimas M (2001) Male dimorphism in the bulb mite, Rhizoglyphus robini: fighters survive better. Ethol Ecol Evol 12:69–79CrossRefGoogle Scholar
  41. Radwan J, Czyż M, Konior M et al (2000) Aggressiveness in two male morphs of the bulb mite Rhizoglyphus robini. Ethology 106:53–62CrossRefGoogle Scholar
  42. Radwan J, Unrug J, Tomkins JL (2002) Status-dependence and morphological trade-offs in the expression of a sexually selected character in the mite, Sancassania berlesei. J Evol Biol 15:744–752CrossRefGoogle Scholar
  43. Radwan J, Unrug J, Śnigórska K et al (2004) Effectiveness of sexual selection in preventing fitness deterioration in bulb mite populations under relaxed natural selection. J Evol Biol 17:94–99PubMedCrossRefGoogle Scholar
  44. Repka J, Gross MR (1995) The evolutionarily stable strategy under individual condition and tactic frequency. J Theor Biol 176:27–31PubMedCrossRefGoogle Scholar
  45. Ryan MJ, Pease CM, Morris MR (1992) A genetic polymorphism in the swordtail Xiphophorus nigrensis. Testing the prediction of equal fitnesses. Am Nat 139:21–31CrossRefGoogle Scholar
  46. Schlichting CD, Pigliucci M (1995) Gene regulation, quantitative genetics and the evolution of reaction norms. Evol Ecol 9:154–168CrossRefGoogle Scholar
  47. Sheldon B (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402PubMedCrossRefGoogle Scholar
  48. Shuster SM, Wade MJ (1991) Equal mating success among male reproductive strategies in a marine isopod. Nature 350:608–610CrossRefGoogle Scholar
  49. Shuster S, Wade MJ (2003) Mating systems and strategies. Princeton University Press, PrincetonGoogle Scholar
  50. Smallegange IM, Coulson T (in press) The stochastic demography of two coexisting male morphs. EcologyGoogle Scholar
  51. Tomkins JL, Hazel W (2007) The status of the conditional evolutionarily stable strategy. Trends Ecol Evol 22:522–528PubMedCrossRefGoogle Scholar
  52. Tomkins JL, LeBas NR, Unrug J et al (2004) Testing the status-dependent ESS model: population variation in fighter expression in the mite Sancassania berlesei. J Evol Biol 17:1377–1388PubMedCrossRefGoogle Scholar
  53. Wedell N (1996) Mate quality affects reproductive effort in a paternally investing species. Am Nat 148:1075–1088CrossRefGoogle Scholar
  54. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Division of BiologyImperial College LondonAscotUK

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