Skip to main content
SpringerLink
Log in

Competitive interactions between parasitoid larvae and the evolution of gregarious development

  • Behavioural Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We report experiments using two closely related species of alysiine braconids directed at understanding how gregarious development evolved in one subfamily of parasitoid wasps. Theoretical models predict that once siblicide between parasitoid wasps has evolved, it can only be lost under stringent conditions, making the transition from solitary to gregarious development exiguous. Phylogenetic studies indicate, however, that gregariousness has independently arisen on numerous occasions. New theoretical models have demonstrated that if gregarious development involves reductions in larval mobility, rather than a lack of fighting ability (as in the older models), the evolution of gregariousness is much more likely. We tested the predictions of the older tolerance models (gregariousness based on non-fighting larval phenotypes) and the reduced mobility models (gregariousness based on non-searching larval phenotypes) by observing larval movement and the outcome of interspecific competition between Aphaereta genevensis (solitary) and A. pallipes (gregarious) under multiparasitism. Differences in larval mobility matched the prediction of the reduced mobility model of gregarious development, with the solitary A. genevensis having larvae that are much more mobile. The proportion of hosts producing the solitary species significantly declined after subsequent exposure to females of the gregarious species. This contradicts the prediction of the older models (fighting vs non-fighting phenotypes), under which any competitive interactions between solitary and gregarious larvae will result in a highly asymmetrical outcome, as the solitary species should be competitively superior. The observed outcome of interspecific competition offers evidence, with respect to this subfamily, in favour of the new models (searching vs non-searching phenotypes).

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. 1a–c
Fig. 2a,b

Similar content being viewed by others

References

  • van Achterberg C (1998) Phaenocarpa helophilae spec. nov. (Hymenoptera: Braconidae), a gregarious parasitoid of Helophilus larvae (Diptera: Syrphidae), with notes on related species. Zool Meded 72:15–27

    Google Scholar 

  • van Baaren J, Boivin G, le Lannic J, Nénon J-P (1997) The male and female first instar larvae of Anaphes victus and A. listronoti (Hymenoptera, Mymaridae). Zoomorphology 117:189–197

    Article  Google Scholar 

  • Belshaw R, Fitton M, Herniou E, Gimeno C, Quicke DLJ (1998) A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Syst Entomol 23:109–123

    Article  Google Scholar 

  • Boivin G (1986) Anaphes sordidatus (Girault) (Hymenoptera: Mymaridae), an egg parasite of the carrot weevil, Listronotus oregonesis (Le Conte). Can Entomol 118:393–394

    Google Scholar 

  • Boivin G, van Baaren J (2000) The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps. Ecol Lett 3:469–474

    Article  Google Scholar 

  • Brodeur J, Boivin G (2004) Functional ecology of immature parasitoids. Annu Rev Entomol 49:27–49

    Article  CAS  PubMed  Google Scholar 

  • Carton Y, Bouletreau M, van Alphen JJM, van Lenteren JC (1986) The Drosophila parasitic wasps. In: Ashburner M, Carson H, Thompson JN (eds) The genetics and biology of Drosophila, vol 3E. Academic, London, pp 347–394

  • Cheplick GP (1992) Sibling competition in plants. J Ecol 80:567–575

    Google Scholar 

  • Crawley MJ (1993) GLIM for ecologists. Blackwell, Oxford

    Google Scholar 

  • Cruz YP (1981) A sterile defender morph in a polyembryonic hymenopterous parasite. Nature 294:446–447

    Google Scholar 

  • Cruz YP (1986) The defender role of the precocious larvae of Copidosomopsis tanytmemus Caltagirone (Encyrtidae, Hymenoptera). J Exp Zool 237:309–318

    Google Scholar 

  • Darwin CR (1859) On the origin of species by means of natural selection. John Murray, London

    Google Scholar 

  • Elgar MA, Crespi BJ (1992) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford

    Google Scholar 

  • Fleming JGW (1992) Polydnaviruses: mutualists and pathogens. Annu Rev Entomol 37:401–425

    Article  CAS  PubMed  Google Scholar 

  • Gimeno C, Belshaw R, Quicke DLJ (1997) Phylogenetic relationships of the Alysiinae/Opiinae (Hymenoptera: Braconidae) and the utility of cytochrome b 16 s and 28 s D2 rRNA. Insect Mol Biol 6:273–284

    Article  CAS  PubMed  Google Scholar 

  • Godfray HCJ (1987) The evolution of clutch size in parasitic wasps. Am Nat 129:221–233

    Article  Google Scholar 

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

    Google Scholar 

  • Godfray HCJ (1995) Evolutionary theory of parent-offspring conflict. Nature 376:133–138

    Article  CAS  PubMed  Google Scholar 

  • Grbíc M, Ode PJ, Strand MR (1992) Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360:254–256

    Article  Google Scholar 

  • Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21

    Article  Google Scholar 

  • Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 97:354–356

    Article  Google Scholar 

  • Hamilton WD (1964a) The genetical evolution of social behaviour I. J Theor Biol 7:1–16

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1964b) The genetical evolution of social behaviour II. J Theor Biol 7:17–52

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232

    Article  Google Scholar 

  • Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature 269:578–581

    Google Scholar 

  • Harvey JA, Kadash K, Strand MR (2000a) Differences in larval feeding behaviour correlate with altered developmental strategies in two parasitic wasps: implications for the size-fitness hypothesis. Oikos 88:621–629.

    Google Scholar 

  • Harvey JA, Corley LS, Strand MR (2000b) Competition induces adaptive shifts in caste ratio of a polyembryonic wasp. Nature 406:183–186

    Article  CAS  PubMed  Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Harvey PH, Partridge L (1987) Murderous mandibles and black holes in hymenopteran wasps. Nature 326:128–129

    Article  Google Scholar 

  • Kfir R, van Hamburg H (1988) Interspecific competition between Telenomus ullyetti (Hymenoptera: Scelionidae) and Trichogrammatoidea lutea (Hymenoptera: Trichogrammatidae) parasitizing eggs of the cotton bollworm Heliothis armiger in the laboratory. Environ Entomol 17:664–670

    Google Scholar 

  • Khoo BK, Forgash AJ, Respicio NC, Ramaswamy SB (1985) Multiple progeny production by gypsy moth parasites Brachymeria spp (Hymenoptera: Chalcididae), following exposure to diflubenzuron. Environ Entomol 14:820–825

    Google Scholar 

  • Laing JE, Corrigan JE (1987) Intrinsic competition between the gregarious parasite Cotesia glomeratus and the solitary parasite Cotesia rubecula (Hymenoptera: Braconidae) for their host Artogeia rapae (Lepidoptera: Pieridae). Entomophaga 32:493–501

    Google Scholar 

  • Lawton JH, Hassell MP (1981) Asymmetrical competition in insects. Nature 289:793–795

    Google Scholar 

  • le Masurier AD (1987) A comparative study of the relationship between host size and brood size in Apanteles spp. (Hymenoptera: Braconidae). Ecol Entomol 12:383–393

    Google Scholar 

  • Mackauer M (1990) Host discrimination and larval competition in solitary endoparasitoids. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Intercept, Andover, pp 41–62

    Google Scholar 

  • Mackauer M, Bai B, Chow A, Danyk T (1992) Asymmetric larval competition between two species of solitary parasitoid wasps: the influence of superparasitism. Ecol Entomol 17:233–236

    Google Scholar 

  • Marktl RC, Stauffer C, Schopf A (2002) Interspecific competition between the braconid endoparasitoids Glyptapanteles porthetriae and Glyptapanteles liparidis in Lymantria dispar larvae. Entomol Exp Appl 105:97–109

    Google Scholar 

  • Marris GC, Casperd J (1996) The relationship between conspecific superparasitism and the outcome of in vitro contests staged between different larval instars of the solitary endoparasitoid Venturia canescens. Behav Ecol Sociobiol 39:61–69

    Article  Google Scholar 

  • Matthews RW (1975) Courtship in parasitic wasps. In: Price PW (ed) Evolutionary strategies of parasitic insects and mites. Plenum, New York, pp 66–82

    Google Scholar 

  • Mayhew PJ (1998a) The evolution of gregariousness in parasitoid wasps. Proc R Soc London B 265:383–389

    Article  Google Scholar 

  • Mayhew PJ (1998b) The life-histories of parasitoid wasps developing in small gregarious broods. Neth J Zool 48:225–240

    Google Scholar 

  • Mayhew PJ, Hardy ICW (1998) Nonsibilicidal behavior and the evolution of clutch size in bethylid wasps. Am Nat 151:409–424

    Article  Google Scholar 

  • Mayhew PJ, van Alphen JJM (1999) Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim Behav 58:131–141

    Article  PubMed  Google Scholar 

  • Miller JC (1982) Life-history of insect parasitoids involved in successful multiparasitism. Oecologia 54:8–9

    Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  • Nénon J-P, Boivin G, le Lannic J, van Baaren J (1995) Functional morphology of the mymariform and sacciform larvae of the egg parasitoid Anaphes victus Huber (Hymenoptera: Mymaridae). Can J Zool 73:996–1000

    Google Scholar 

  • Nicholson AJ (1954) An outline of the dynamics of animal populations. Aust J Zool 2:9–65

    Google Scholar 

  • Nixon GEL (1965) A reclassification of the tribe Microgasterini (Hymenoptera: Braconidae). Bull Br Museum Nat Hist Entomol Suppl 2:1–284

    Google Scholar 

  • Ode PJ, Rosenheim JA (1998) Sex allocation and the evolutionary transition between solitary and gregarious parasitoid development. Am Nat 152:757–761

    Article  Google Scholar 

  • Pexton JJ, Mayhew PJ (2001) Immobility: the key to family harmony? Trends Ecol Evol 16:7–9

    Article  PubMed  Google Scholar 

  • Pexton JJ, Rankin DJ, Dytham C, Mayhew PJ (2003) Asymmetric larval mobility and the evolutionary transition from siblicide to nonsiblicidal behavior in parasitoid wasps. Behav Ecol 14:182–193

    Article  Google Scholar 

  • Quicke DLJ (1993) The polyphyletic origin of endoparasitism in the cyclostome lineages of Braconidae (Hymenoptera): a reassessment. Zool Meded 67:159–177

    Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, New York

    Google Scholar 

  • Quicke DLJ, van Achterberg C (1990) Phylogeny of the subfamilies of the Braconidae (Hymenoptera: Ichneumonoidea). Zool Verh 285:1–95

    Google Scholar 

  • Rosenheim JA (1993) Single sex broods and the evolution of nonsiblicidal parasitoid wasps. Am Nat 141:90–104

    Article  Google Scholar 

  • Salt G (1961) Competition among insect parasitoids. Symp Soc Exp Biol 15:96–119

    Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Shaw MR, Huddleston T (1991) Classification and biology of Braconid Wasps (Hymenoptera: Braconidae): handbooks for the identification of British insects. Natural History Museum, London

    Google Scholar 

  • Skinner SW (1985) Clutch size as an optimal foraging problem for insects. Behav Ecol Sociobiol 17:231–238

    Article  CAS  PubMed  Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Strand MR (1986) The physiological interactions of parasitoids with their hosts and their influence on reproduction strategies. In: Waage J, Greathead D (eds) Insect parasitoids. Academic, London, pp 97–136

    Google Scholar 

  • Strand MR, Vinson SB (1984) Facultative hyperparasitism by the egg parasitoid Trichogramma pretiosum (Hymenoptera, Trichogrammatidae). Ann Entomol Soc Am 77:679–686

    Google Scholar 

  • Strand MR, Johnson JA, Culin JD (1990) Intrinsic interspecific competition between the polyembryonic parasitoid Copidosoma floridanum and solitary endoparasitoid Microplitis demolitor in Pseudoplusia includens. Entomol Exp Appl 55:275–284

    Google Scholar 

  • van Strien-van Liempt WTFH (1983) The competition between Asobara tabida Nees and Leptopilina heterotoma (Thomson) in multiparasitized hosts. I. The course of competition. Neth J Zool 33:125–163

    Google Scholar 

  • Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264

    Google Scholar 

  • Utsunomiya A, Iwabuchi K (2002) Interspecific competition between the polyembryonic wasp Copidosoma floridanum and the gregarious endoparasitoid Glyptapanteles pallipes. Entomol Exp Appl 104:353–362

    Google Scholar 

  • Vinson SB, Hegazi EM (1998) A possible mechanism for the physiological suppression of conspecific eggs and larvae following superparasitism by solitary endoparasitoids. J Insect Physiol 44:703–712

    Article  CAS  PubMed  Google Scholar 

  • Waage JK, Godfray HCL (1985) Reproductive strategies and population ecology of insect parasitoids. In: Sibly RM, Smith RH (eds) Behavioural ecology: ecological consequences of adaptive behaviour. Blackwell, Oxford, pp 449–470

    Google Scholar 

  • West SA, Murray MG, Machado CA, Griffin AS, Herre EA (2001) Testing Hamilton’s rule with competition between relatives. Nature 409:510–513

    Article  CAS  PubMed  Google Scholar 

  • West SA, Pen I, Griffin AS (2002) Co-operation and competition between relatives. Science 296:72–75

    Article  CAS  PubMed  Google Scholar 

  • Wharton RA (1977) New World Aphaereta species (Hymenoptera: Braconidae: Alysiinae), with a discussion of terminology used in the tribe Alysiini. Ann Entomol Soc Am 70:782–803

    Google Scholar 

  • Wharton RA (1980) Review of the nearctic Alysiini species (Hymenoptera, Braconidae) with discussion of generic relationships within the tribe. Univ California Publ Entomol 88:1–112

    Google Scholar 

  • Wharton RA (1984) Biology of the Alysiini (Hymenoptera, Braconidae), parasitoids of cyclorrhaphous Diptera. Tech Monogr Tex Agric Exp Stat 11:1–39

    Google Scholar 

  • Whitfield JB (1997) Subfamily Microgastrinae. In: Wharton RA, Marsh PM, Sharkey MJ (eds) Manual of the new world genera of the family Braconidae (Hymenoptera). The International Society of Hymenopterists, Washington, pp 332–364

    Google Scholar 

  • Williams GC (1992) Natural selection: domains, levels and challenges. Oxford University Press, Oxford

    Google Scholar 

  • Williams GC, Williams DC (1957) Natural selection of individually harmful social adaptations among sibs with special reference to social insects. Evolution 11:32–39

    Article  Google Scholar 

  • Wilson DS, Dugatkin LA (1997) Group selection and assortative interactions. Am Nat 149:336–351

    Article  Google Scholar 

  • Wilson DS, Pollock GB, Dugatkin LA (1992) Can altruism evolve in purely viscous populations? Evol Ecol 6:331–341

    Google Scholar 

Download references

Acknowledgements

J.J.P. was funded by a NERC studentship. The authors also warmly thank Jeremy Searle, Stu West, and an anonymous referee for constructive comments on a previous version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, University of York, PO Box 373, York, YO10 5 YW, UK

    John J. Pexton & Peter J. Mayhew

Authors
  1. John J. Pexton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter J. Mayhew
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter J. Mayhew.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pexton, J.J., Mayhew, P.J. Competitive interactions between parasitoid larvae and the evolution of gregarious development. Oecologia 141, 179–190 (2004). https://doi.org/10.1007/s00442-004-1659-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-004-1659-3

Keywords

Search

Navigation