Skip to main content
SpringerLink
Log in

Divergent life history strategies in congeneric hyperparasitoids

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Life histories can reveal important information on the performance of individuals within their environment and how that affects evolutionary change. Major trait changes, such as trait decay or loss, may lead to pronounced differences in life history strategies when tight correlations between traits exist. Here, we show that three congeneric hyperparasitoids (Gelis agilis, Gelis acarorum and Gelis areator) that have diverged in wing development and reproductive mode employ markedly different life history strategies. Potential fecundity of Gelis sp. varied, with the wingless G. acarorum maturing a much higher number of eggs throughout life compared with the other two species. Realized lifetime fecundity, in terms of total offspring number was, however, highest for the winged G. areator. The parthenogenic G. agilis invests its resources solely in females, whilst the sexually reproducing species both invested heavily in males to reduce competitive pressures for their female offspring. Longevity also differed between species, as did the direction of the reproduction-longevity trade-off, where reproduction is heavily traded off against longevity only in the asexual G. agilis. Resting metabolic rates also differed between the winged and wingless species, with the highest metabolic rate observed in the winged G. areator. Overall, these geline hyperparasitoids showed considerable divergence in life history strategies, both in terms of timing and investment patterns. Major trait changes observed between closely related species, such as the loss of wings and sexual reproduction, may contribute to the divergence in key life history traits.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Boivin G, Gauvin M-J (2009) Egg size affects larval performance in a coleopteran parasitoid. Ecol Entomol 34:240–245

    Article  Google Scholar 

  • Boratyński Z, Koteja P (2010) Sexual and natural selection on body mass and metabolic rates in free-living bank voles. Funct Ecol 24:1252–1261

    Article  Google Scholar 

  • Bourchier R, Nealis V (1992) Patterns of hyperparasitism of Cotesia melanoscela (Hymenoptera, Braconidae) in southern Ontario. Environ Entomol 21:907–912

    Article  Google Scholar 

  • Burton T, Killen SS, Armstrong JD et al (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278:3465–3473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charnov EL, Los-den Hartogh RL, Jones WT et al (1981) Sex ratio evolution in a variable environment. Nature 289:27–33

    Article  CAS  PubMed  Google Scholar 

  • Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163–165

    Article  CAS  PubMed  Google Scholar 

  • Clark RM, Zera AJ, Behmer ST (2015) Nutritional physiology of life-history trade-offs: how food protein–carbohydrate content influences life-history traits in the wing-polymorphic cricket Gryllus firmus. J Exp Biol 15:298–308

    Article  Google Scholar 

  • Denno RF, Olmstead KL, McCloud ES (1989) Reproductive cost of flight capability: a comparison of life history traits in a wing dimorphic planthoppers. Ecol Entomol 14:31–44

    Article  Google Scholar 

  • Development Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Einum S, Fleming I (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 57:565–567

    Article  Google Scholar 

  • Flatt T (2011) Survival costs of reproduction in Drosophila. Exp Gerontol 46:369–375

    Article  PubMed  Google Scholar 

  • Fox CW (1993) The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia 96:139–146

    Article  Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Ann Rev Entomol 45:341–369

    Article  CAS  Google Scholar 

  • Gems D, Riddle D (1996) Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature 379:723–725

    Article  CAS  PubMed  Google Scholar 

  • Gibbs AM, Lace LA, Jones MJ et al (2005) Egg size-number trade-off and a decline in oviposition site choice quality: female Pararge aegeria butterflies pay a cost of having males present at oviposition. J Insect Sci 5:1–9

    Article  Google Scholar 

  • Gilbert JDJ, Manica A (2010) Parental care trade-offs and life history relationships in insects. Am Nat 176:212–226

    Article  PubMed  Google Scholar 

  • Gillooly JF, Brown JH, West GB et al (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  PubMed  Google Scholar 

  • Giron D, Casas J (2003) Mothers reduce egg provisioning with age. Ecol Lett 6:273–277

    Article  Google Scholar 

  • Giron D, Rivero A, Mandon N et al (2002) The physiology of host feeding in parasitic wasps: implications for survival. Funct Ecol 16:750–757

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, West Sussex

    Google Scholar 

  • Gómez-Marco F, Urbaneja A, Jaques JA et al (2015) Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control? Biol Control 81:111–121

    Article  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  CAS  PubMed  Google Scholar 

  • Harvey JA (2000) Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness. Ecol Entomol 25:267–278

    Article  Google Scholar 

  • Harvey JA (2008) Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Evol Ecol 22:153–166

    Article  Google Scholar 

  • Harvey JA, Witjes LM (2005) Comparing and contrasting life history and development strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Appl Entomol Zool 40:309–316

    Article  Google Scholar 

  • Harvey JA, Wagenaar R, Gols R (2011a) Differing host exploitation efficiencies in two hyperparasitoids: When is a “match made in heaven”? J Insect Behav 24:282–292

    Article  PubMed  PubMed Central  Google Scholar 

  • Harvey JA, Pashalidou F, Soler R et al (2011b) Intrinsic competition between two secondary hyperparasitoids results in temporal trophic switch. Oikos 120:226–233

    Article  Google Scholar 

  • Harvey JA, Cloutier J, Visser B et al (2012) The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps. J Insect Physiol 58:816–823

    Article  CAS  PubMed  Google Scholar 

  • Harvey JA, Snaas H, Malcicka M et al (2014) Small-scale spatial resource partitioning in a hyperparasitoid community. Arth Plant Int 8:393–401

    Article  Google Scholar 

  • Harvey JA, Gols R, Snaas H et al (2015) Host preference and offspring performance are linked in three congeneric hyperparasitoid species. Ecol Entomol 40:114–122

    Article  Google Scholar 

  • Hoffman AA, Hallas R, Sinclair C, Partridge L (2001) Rapid loss of stress resistance in Drosophila melanogaster under adaptation to laboratory culture. Evolution 55:436–438

    Article  Google Scholar 

  • Hořák D, Klvaňa P, Albrecht T (2008) Why there is no negative correlation between egg size and number in the Common Pochard? Acta Oecol 33:197–202

    Article  Google Scholar 

  • Hsu J (1996) Multiple comparisons: theory and methods. Chapman & Hall, New York

    Book  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R et al (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213

    Article  CAS  PubMed  Google Scholar 

  • Hurst L, Peck J (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol Evol 11:46–52

    Article  CAS  PubMed  Google Scholar 

  • Jackson DM, Trayhurn P, Speakman JR (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J Anim Ecol 70:633–640

    Article  Google Scholar 

  • Jervis MA, Ferns P (2011) Towards a general perspective on life-history evolution and diversitfication in parasitoid wasps. Biol J Linn Soc 104:443–461

    Article  Google Scholar 

  • Jervis MA, Kidd NAC (1986) Host-feeding strategies in hymenopteran parasitoids. Biol Rev 61:395–434

    Article  Google Scholar 

  • Jervis MA, Heimpel GE, Ferns PN et al (2001) Life-history strategies in parasitoid wasps: a comparative analysis of “ovigeny”. J Anim Ecol 70:442–458

    Article  Google Scholar 

  • Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation and utilization in parasitoid reproductive strategies. Ann Rev Entomol 53:361–385

    Article  CAS  Google Scholar 

  • Jervis MA, Moe A, Heimpel GE (2012) The evolution of parasitoid fecundity: a paradigm under scrutiny. Ecol Lett 15:357–364

    Article  PubMed  Google Scholar 

  • Kawecki TJ (2008) Adaptation to marginal habitats. Ann Rev Ecol Evol Syst 39:321–342

    Article  Google Scholar 

  • Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512

    Article  CAS  PubMed  Google Scholar 

  • King B (1987) Offspring sex ratios in parasitoid wasps. Q Rev Biol 62:367–396

    Article  Google Scholar 

  • King EG, Roff DA, Fairbairn DJ (2011) Trade-off acquisition and allocation in Gryllus firmus: a test of the Y model. J Evol Biol 24:256–264

    Article  CAS  PubMed  Google Scholar 

  • Kolm N, Goodwin NB, Balshine S et al (2006) Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size. J Evol Biol 19:76–84

    Article  CAS  PubMed  Google Scholar 

  • Kramer M, Templeton A (2001) Life history changes that accompany the transition from sexual to parthenogenic reproduction in Drosophila mercatorum. Evolution 55:748–761

    Article  CAS  PubMed  Google Scholar 

  • Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA (2009) Relaxed selection in the wild. Trends Ecol Evol 24:487–496

    Article  PubMed  Google Scholar 

  • Lamb R, Willey R (1979) Are parthenogenetic and related bisexual insects equal in fertility? Evolution 33:774–775

    Article  Google Scholar 

  • Laurenne N (2008) Phylogeny of a taxonomically difficult group and evolution of host location mechanism. PhD thesis. Faculty of the Biosciences of the University of Helsinki, Helsinki

  • Le Lann C, Wardziak T, van Baaren J et al (2011) Thermal plasticity of metabolic rates linked to life-history traits and foraging behaviour in a parasitic wasp. Funct Ecol 25:641–651

    Article  Google Scholar 

  • Le Lann C, Visser B, van Baaren J et al (2012) Comparing resource exploitation and allocation of two closely related aphid parasitoids sharing the same host. Evol Ecol 26:79–94

    Article  Google Scholar 

  • Le Lann C, Lodi M, Ellers J (2014a) Thermal change alters the outcome of behavioural interactions between antagonistic partners. Ecol Entomol 39:578–588

    Article  Google Scholar 

  • Le Lann C, Visser B, Mériaux M et al (2014b) Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species. Oecologia 174:967–977

    Article  PubMed  Google Scholar 

  • Lehtonen J, Jennions MD, Kokko H (2012) The many costs of sex. Trends Ecol Evol 27:172–176

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Libert P (2010) Contribution a la connaissance de l’entomofaune d’un village famennien. I. Cryptinae (Hymenoptera: Ichneumonidae). Faun Entomol 63:47–82

    Google Scholar 

  • Madec L (2000) Phenotypic plasticity in reproductive traits: importance in the life history of Helix aspersa (Mollusca: Helicidae) in a recently colonized habitat. Biol J Linn Soc 69:25–39

    Article  Google Scholar 

  • Martin TE (2015) Age-related mortality explains life history strategies of tropical and temperate songbirds. Science 349:966–970

    Article  CAS  PubMed  Google Scholar 

  • Mayhew PJ, Blackburn TM (1999) Does development mode organize life-history traits in the parasitoid Hymenoptera? J Anim Ecol 68:906–916

    Article  Google Scholar 

  • McIntyre G, Gooding R (2000) Egg size, contents, and quality: maternal-age and-size effects on house fly eggs. Can J Zool 78:1544–1551

    Article  Google Scholar 

  • Mole S, Zera A (1993) Differential allocation of resources underlies the dispersal-reproduction trade-off in the wing-dimorphic cricket, Gryllus rubens. Oecologia 93:121–127

    Article  Google Scholar 

  • Partridge L, Gems D (2002) Mechanisms of ageing: Public or private? Nat Rev Genet 3:165–175

    Article  CAS  PubMed  Google Scholar 

  • Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic hymenoptera. Ann Rev Entomol 51:233–258

    Article  CAS  Google Scholar 

  • Poelman EH, Bruinsma M, Zhu F et al (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol 10:e1001435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preziosi RF, Fairbairn DJ, Roff DA et al (1996) Body size and fecundity in the waterstrider Aquarius remigis: a test of Darwin’s fecundity advantage hypothesis. Oecologia 108:424–431

    Article  Google Scholar 

  • Price PW (1973) Reproductive strategies in parasitoid wasps. Am Nat 107:684–693

    Article  Google Scholar 

  • Reinhold K (1999) Energetically costly behaviour and the evolution of resting metabolic rate in insects. Funct Ecol 13:217–224

    Article  Google Scholar 

  • Rivero A, West SA (2002) The physiological costs of being small in a parasitic wasp. Evol Ecol Res 4:407–420

    Google Scholar 

  • Rivers DB, Denlinger DL (1994) Redirection of metabolism in the flesh fly, Sarcophaga bullata, following envenomation by the ectoparasitoid Nasonia vitripennis and correlation of metabolic effects with the diapause status of the host. J Insect Physiol 40:207–215

    Article  CAS  Google Scholar 

  • Rivers DB, Denlinger DL (1995) Venom-induced alterations in fly lipid metabolism and its impact on larval development of the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). J Invertebr Pathol 66:104–110

    Article  CAS  Google Scholar 

  • Schwarzkopf L, Blows M, Caley M (1999) Life-history consequences of divergent selection on egg size in Drosophila melanogaster. Am Nat 154:333–340

    Article  PubMed  Google Scholar 

  • Shaw MR (2006) Habitat considerations for parasitic wasps (Hymenoptera). J Insect Conserv 10:117–127

    Article  Google Scholar 

  • Simmons FH, Bradley TJ (1997) An analysis of resource allocation in response to dietary yeast in Drosophila melanogaster. J Insect Physiol 43:779–788

    Article  CAS  PubMed  Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486

    Article  CAS  PubMed  Google Scholar 

  • Tatar M (2010) Reproductive aging in invertebrate genetic models. Ann NY Acad Sci 1204:149–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor V (1981) The adaptive and evolutionary significance of wing polymorphism and parthenogenesis in Ptinella Motschulsky (Coleoptera: Ptiliidae). Ecol Entomol 6:89–98

    Article  Google Scholar 

  • Timi JT, Lanfranchi AL, Poulin R (2005) Is there a trade-off between fecundity and egg volume in the parasitic copepod Lernanthropus cynoscicola? Parasitol Res 95:1–4

    Article  PubMed  Google Scholar 

  • Van Voorhies WA, Ward S (1999) Genetic and environmental conditions that increase longevity in Caenorhabditis elegans decrease metabolic rate. Proc Natl Acad Sci USA 96:11399–11403

    Article  PubMed  PubMed Central  Google Scholar 

  • Visser B, Lann C, Snaas H et al (2014) Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp. Behav Ecol Sociobiol 68:105–113

    Article  Google Scholar 

  • Warne RW, Charnov EL (2008) Reproductive allometry and the size-number trade-off for lizards. Am Nat 172:E80–E98

    Article  PubMed  Google Scholar 

  • West S (2009) Sex allocation. Princeton University Press, West Sussex

    Book  Google Scholar 

  • Williams TD (2001) Experimental manipulation of female reproduction reveals an intraspecific egg size-clutch size trade-off. Proc R Soc B 268:423–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuur A, Ieno E, Walker N et al (2009) Mixed effect models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We would like to thank Roel Wagenaar for his help in rearing of the hyperparasitoids and three anonymous referees for their constructive comments on earlier drafts of this manuscript. B. V. is further grateful to Louise Vet and Wim van der Putten for their hospitality to work in their institute and department. C. L. L. was supported by the IEF People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program (FP7/2007-2013) under REA grant agreement n° 274386, project COEVOLCLIM. B. V. was supported by a Netherlands Organisation for Scientific Research Rubicon fellowship with Grant No. 815.12.014 and the IEF People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program (FP7/2007–2013) under REA grant agreement n° 298457, project ECOLOGY&LIPOGENESIS.

Author information

Authors and Affiliations

  1. Department of Terrestrial Ecology, Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands

    Bertanne Visser, Helen Snaas & Jeffrey A. Harvey

  2. Evolutionary Ecology and Genetics Group, Biodiversity Research Centre, Earth and Life Institute, Université Catholique de Louvain, Croix du Sud 4, 1348, Louvain-la-Neuve, Belgium

    Bertanne Visser

  3. Unité Mixte de Recherche CNRS 6553, ECOBIO, Université de Rennes 1, 35042, Rennes Cedex, France

    Cécile Le Lann

  4. Department of Ecological Science, VU University Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

    Cécile Le Lann & Jeffrey A. Harvey

  5. Department of Functional and Evolutionary Ecology, Estación Experimental de Zonas Áridas (EEZA-CSIC), Carretera de Sacramento, s/n, La Cañada de San Urbano, 04120, Almería, Spain

    Oriol Verdeny-Vilalta

Authors
  1. Bertanne Visser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cécile Le Lann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helen Snaas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oriol Verdeny-Vilalta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeffrey A. Harvey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bertanne Visser.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Visser, B., Le Lann, C., Snaas, H. et al. Divergent life history strategies in congeneric hyperparasitoids. Evol Ecol 30, 535–549 (2016). https://doi.org/10.1007/s10682-016-9819-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-016-9819-6

Keywords

Search

Navigation