Skip to main content

Advertisement

Log in

Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly

  • Physiological Ecology - Original Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Life history characteristics and resulting fitness consequences manifest not only in an individual experiencing environmental conditions but also in its offspring via trans-generational effects. We conducted a set of experiments to assess the direct and trans-generational effects of food deprivation in the Glanville fritillary butterfly Melitaea cinxia. Food availability was manipulated during the final stages of larval development and performance was assessed during two generations. Direct responses to food deprivation were relatively minor. Food-deprived individuals compensated, via increased development time, to reach a similar mass as adults from the control group. Delayed costs of compensatory growth were observed, as food-deprived individuals had either reduced fecundity or lifespan depending on the type of feeding treatment they had experienced (intermittent vs. continuous). Female food deprivation did not directly affect her offspring’s developmental trajectory, but the way the offspring coped with food deprivation. Offspring of mothers from control or intermittent starvation treatments reached the size of those in the control group via increased development time when being starved. In contrast, offspring of mothers that had experienced 2 days of continuous food deprivation grew even larger than control animals, when deprived of food themselves. Offspring of food-deprived Glanville fritillary initially showed poor immune response to parasitism, but not later on in development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal AA (2002) Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83:3408–3415

    Article  Google Scholar 

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defenses in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Alleyne M, Wiedenmann RN (2001) Encapsulation and hemocyte numbers in three lepidopteran stemborers parasitized by Cotesia flavipes-complex endoparasitoids. Entomol Exp Appl 100:279–293

    Article  Google Scholar 

  • Baldal EA, Brakefield PM, Zwaan BJ (2006) Multitrait evolution in lines of Drosophila melanogaster selected for increased starvation resistance: the role of metabolic rate and implications for the evolution of longevity. Evolution 60:1435–1444

    PubMed  Google Scholar 

  • Barrett ELB, Hunt J, Moore AJ, Moore PJ (2009) Separate and combined effects of nutrition during juvenile and sexual development on female life-history trajectories: the thrifty phenotype in a cockroach. Proc R Soc Lond B 276:3257–3264

    Article  Google Scholar 

  • Bashey F (2006) Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata. Evolution 60:348–361

    PubMed  Google Scholar 

  • Bauer E, Trenczek T, Dorn S (1998) Instar-dependent hemocyte changes in Pieris brassicae after parasitization by Cotesia glomerata. Entomol Exp Appl 88:49–58

    Article  Google Scholar 

  • Bauerfeind SS, Fischer K (2005a) Effects of adult-deprived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly. J Insect Physiol 51:545–554

    Article  PubMed  CAS  Google Scholar 

  • Bauerfeind SS, Fischer K (2005b) Effects of food stress and density in different life stages on reproduction in a butterfly. Oikos 111:514–524

    Article  Google Scholar 

  • Beckage NE, Thompson SA, Federici BA (eds) (1993) Parasites and pathogens of insects. Academic, New York

    Google Scholar 

  • Bishop NA, Guarente L (2007) Genetic links between diet and lifespan:shared mechanisms from yeast to humans. Nat Rev Genet 8:835–844

    Article  PubMed  CAS  Google Scholar 

  • Boggs CL (2009) Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol 23:27–37

    Article  Google Scholar 

  • Boggs CL, Freeman KD (2005) Larval food limitation in butterflies: effects of adult resource allocation and fitness. Oecologia 144:353–361

    Article  PubMed  Google Scholar 

  • Boggs CL, Ross CL (1993) The effect of adult food limitation on the life-history traits in Speyeria mormonia (Lepidoptera: Nymphalidae). Ecology 74:433–441

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Bukovinszky T et al (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308

    Article  PubMed  Google Scholar 

  • Criscuolo F, Monaghan P, Nasir L, Metcalfe NB (2008) Early nutrition and phenotypic development: “catch-up” growth leads to elevated metabolic rate in adulthood. Proc R Soc Lond B 275:1565–1570

    Article  Google Scholar 

  • Dmitriew C, Rowe L (2007) Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis). J Evol Biol 20:1298–1310

    Article  PubMed  CAS  Google Scholar 

  • Dmitriew C, Rowe L (2011) The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS One 6:e17399

    Article  PubMed  CAS  Google Scholar 

  • Esperk T, Tammaru T (2010) Size compensation in moth larvae: attention to larval instars. Physiol Entomol 35:222–230

    Article  Google Scholar 

  • Fox CW, Mousseau TA (1998) Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 159–177

    Google Scholar 

  • Fox CW, Czesak ME, Savalli UM (1999) Environmentally-based maternal effects on development time in the seed beetle, Stator pruininus (Coleoptera: Bruchidae): consequences of larval density. Environ Entomol 28:217–223

    Google Scholar 

  • Garcia-Barros E (2000) Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperioidea). Biol J Linn Soc 70:251–284

    Article  Google Scholar 

  • Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643

    Article  PubMed  CAS  Google Scholar 

  • Hafer N, Ebil S, Uller T, Pike N (2011) Transgenerational effects of food availability on age at maturity and reproductive output in an asexual collembolan species. Biol Lett 7:755–758

    Article  PubMed  Google Scholar 

  • Hanski I, Meyke E (2005) Large-scale dynamics if the Glanville fritillary butterfly: landscape structure, population processes, and weather. Ann Zool Fenn 42:379–395

    Google Scholar 

  • Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life history trade-offs in a butterfly metapopulation. J Anim Ecol 75:91–100

    Article  PubMed  Google Scholar 

  • Harbison ST, Chang S, Kamdar KP, Mackay TFC (2005) Quantitative genomics of starvation stress resistance in Drosophila. Genome Biol 6:R36

    Article  PubMed  Google Scholar 

  • Hector KL, Nakagawa S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol. doi:10.1111/j.1365-2656.2011.01942.x

    PubMed  Google Scholar 

  • Helle H, Koskela E, Mappes T (2012) Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history. J Anim Ecol. doi:10.1111/j.1365-2656.2011.01937.x

    PubMed  Google Scholar 

  • Hellmann J (2002) The effect of an environmental change on mobile butterfly larvae and the nutritional quality of their hosts. J Anim Ecol 71:925–936

    Article  Google Scholar 

  • Jimenez-Perez A, Wang Q (2004) Effect of body weight on reproductive performance in Cnephasia jactatana (Lepidoptera: Tortricidae). J Insect Behav 17:511–522

    Article  Google Scholar 

  • Kankare M, Stefanescu C, Van Nouhuys S, Shaw MR (2005) Host specialization by Cotesia wasps (Hymenoptera: Braconidae) parasitizing species-rich Melitaeini (Lepidoptera: Nymphalidae) communities in north-eastern Spain. Biol J Linn Soc 86:45–65

    Article  Google Scholar 

  • Krug P, Zimmer R (2000) Developmental dimorphism: consequences for larval behavior and dispersal potential in a marine gastropod. J Exp Biol 203:1741–1754

    PubMed  CAS  Google Scholar 

  • Kuussaari M, Singer M, Hanski I (2000) Local specialization and landscape-level influence on host use in a herbivorous insect. Ecology 81:2177–2187

    Article  Google Scholar 

  • Kuussaari M, van Nouhuys S, Hellmann J, Singer M (2004) Larval biology. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, Oxford, pp 138–160

    Google Scholar 

  • Lackie AM (1988) Haemocyte behavior. Adv Insect Physiol 21:85–178

    Article  CAS  Google Scholar 

  • Laurentz M, Reudler JH, Mappes J, Friman V, Ikonen S, Lindstedt C (2012) Diet quality can play a critical role in defence efficacy against parasitoids and pathogens in the Glanville fritillary (Melitaea cinxia). J Chem Ecol 38(1):116–125

    Article  PubMed  CAS  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309

    Article  PubMed  CAS  Google Scholar 

  • Lei GC, Vikberg V, Nieminen M, Kuussaari M (1997) The parasitoid complex attacking the Finnish populations of Glanville fritillary Melitaea cinxia (Lep: Nymphalidae), an endangered butterfly. J Nat Hist 31:635–648

    Article  Google Scholar 

  • Liefting M, Hoffmann AA, Ellers J (2009) Plasticity versus environmental canalization: population differences in thermal responses along a latitudinal gradient in Drosophila serrata. Evolution 63:1954–1963

    Article  PubMed  Google Scholar 

  • Lopez-Maury L, Marguerat S, Bähler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9:583–593

    Article  PubMed  CAS  Google Scholar 

  • Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418–427

    Article  PubMed  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221

    Article  PubMed  CAS  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17:551–557

    Article  Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B 363:1635–1645

    Article  Google Scholar 

  • Monaghan P, Heidinger BJ, D’Alba L, Evans NP, Spencer KA (2011) For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners. Proc R Soc Lond B 279:709–714

    Article  Google Scholar 

  • Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168

    Article  PubMed  CAS  Google Scholar 

  • Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annu Rev Entomol 36:511–534

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  PubMed  CAS  Google Scholar 

  • O’Brien DM, Boggs CL, Fogel ML (2004) Making eggs from nectar: the role of life history and dietary carbon turnover in butterfly reproductive resource allocation. Oikos 105:279–291

    Article  Google Scholar 

  • Okech SHO, Overholt WA (1996) Comparative biology of Cotesia chilonis (Hymenoptera: Braconidae) on selected African gramineous stemborers. Biocontrol Sci Technol 6:595–602

    Article  Google Scholar 

  • Pachauri RK, Reisinger A (eds) (2007) IPCC, Climate change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC, Geneva, Switzerland

  • Pakarinen S (2011) Host-parasitoid relationship in different Cotesia melitaearum and Melitaea cinxia populations around the Baltic Sea. MSc thesis, University of Helsinki, Helsinki

  • Parsons PA (1993) Evolutionary adaptations and stress: energy budgets and habitats preferred. Behav Genet 23:231–238

    Article  PubMed  CAS  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Grylluis bimaculatus. Funct Ecol 19:323–330

    Article  Google Scholar 

  • Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21:408–421

    Article  Google Scholar 

  • Saastamoinen M (2007) Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecol Entomol 32:235–242

    Article  Google Scholar 

  • Saastamoinen M, van Nouhuys S, Nieminen M, O’Hara B, Suomi J (2007) Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann Zool Fenn 44:70–80

    Google Scholar 

  • Saastamoinen M, Ikonen S, Hanski I (2009) Significant effects of Pgi genotype and body reserves on lifespan in the Glanville fritillary butterfly. Proc R Soc Lond B 276:1313–1322

    Article  CAS  Google Scholar 

  • Saastamoinen M, van der Sterren D, Vastenhout N, Zwaan BJ, Brakefield PM (2010) Predictive adaptive responses: condition-dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. Am Nat 176:686–698

    Article  PubMed  Google Scholar 

  • Salinas S, Munch SB (2011) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163

    Article  PubMed  Google Scholar 

  • Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366

    Article  Google Scholar 

  • Schmidt O, Theopold U, Strand M (2001) Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. Bioessays 23:344–351

    Article  PubMed  CAS  Google Scholar 

  • Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14

    Article  CAS  Google Scholar 

  • van Nouhuys S, Hanski I (2005) Metacommunities of butterflies, their host plants and their parasitoids. In: Holyoak M, Leibold MA, Holt RD (eds) Metacommunities: spatial dynamics and ecological communities. University of Chicago Press, Chicago, pp 99–121

    Google Scholar 

  • van Nouhuys S, Laine A-L (2008) Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly. Proc R Soc Lond B 275:787–795

    Article  Google Scholar 

  • van Nouhuys S, Lei GC (2004) Parasitoid-host metapopulation dynamics: the causes and consequences of phenological asynchrony. J Anim Ecol 73:526–535

    Article  Google Scholar 

  • van Nouhuys S, Punju E (2010) Coexistence of competing parasitoids: which is the fugitive and where does it hide? Oikos 119:61–70

    Article  Google Scholar 

  • van Nouhuys S, Singer M, Nieminen M (2003) Spatial and temporal patterns of caterpillar performance and the suitability of two host plant species. Ecol Entomol 28:193–202

    Article  Google Scholar 

  • Vet LEM, Lewis WJ, Papaj DR, van Lenteren JC (1990) A variable response model for parasitoid foraging behavior. J Insect Behav 31:471–490

    Article  Google Scholar 

  • Vinson SB (1976) Host selection by insect parasitoids. Annu Rev Entomol 21:109–134

    Article  Google Scholar 

  • Yoder JA, Tank JL, Rellinger EJ (2006) Evidence of a maternal effect that protects against water stress in larvae of the American dog tick, Dermacentor variabilis (Acari: Ixodidae). J Insect Physiol 52:1034–1042

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Lea Heikkinen, Terhi Lahtinen, Linda Peltola and Suvi Ikonen for their assistance in the experiments. We thank Ilkka Hanski, Klaus Fischer, and two anonymous referees for their useful comments on the manuscript. This research was funded by the Academic Academy of Finland Grants (Nos. 132697 to M.S., and 213547 and 130958 to S.v.N.) and by the European Research Council Advanced Grant (232826 to I. Hanski).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Saastamoinen.

Additional information

Communicated by Klaus Fischer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Appendix A (DOCX 15 kb)

Supplementary Appendix B (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saastamoinen, M., Hirai, N. & van Nouhuys, S. Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly. Oecologia 171, 93–104 (2013). https://doi.org/10.1007/s00442-012-2412-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2412-y

Keywords

Navigation