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Clutch size adjustment, information use and the evolution of gregarious development in parasitoid wasps

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Abstract

As larvae, solitary species of parasitoid wasps eliminate rivals, including sibs, through contest competition. In gregarious species, larvae tolerate each other and several individuals can develop from a single host. We report experiments on two congeneric braconid species aimed at understanding how gregarious development evolved in one genus, and the consequences of larval interactions for parental behavior. In the transition from solitary to gregarious development, one possible intermediate stage is if solitary species frequently lay more than one egg per host. If the risk of conspecific superparasitism (another female of the same species oviposits into a single host) is high, optimal clutch size theory predicts the laying of multiple-egg clutches, because a female will increase the probability of the surviving larva being her own. Under the same conditions, theory predicts that gregarious species should reduce their clutch size. In our experiments, the solitary Aphaereta genevensis increased their clutch size under the risk of intraspecific competition for hosts whilst the gregarious A. pallipes reduced their clutch size, as predicted. In A. genevensis, the response to the risk of competition was dependent upon body size, being greatest amongst small females. In A. pallipes, the response did not depend on female body size, but clutch size increased with body size in all treatments, unlike in A. genevensis. Under the risk of competition from the other species, the response differed relative to the intraspecific treatments and differed between species. Thus, our data suggest that: (1) competition for hosts may have contributed to the evolution of gregarious development in this genus; (2) female wasps can combine information from both external and internal cues in complex ways during clutch size adjustment; and (3) the social environment may alter the adaptive response to both external and internal cues in adult females.

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References

  • Achterberg C van (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 

  • Atkinson WD, Shorrocks B (1981) Competition on a divided and ephemeral resource: a simulation model. J Anim Ecol 50:461–471

    Google Scholar 

  • Bakker K, van Alphen JJM, van Batenberg FHD, van der Hoeven N, Nell HW, van Strien-van Liempt WTFH, Turlings TCJ (1985) The function of host discrimination and superparasitism in parasitoids. Oecologia 67:572–576

    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, 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 

  • Chau A, Mackauer M (1999) Self-superparasitism in the solitary parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiidae): proximate mechanisms. Can Entomol 131:769–777

    Google Scholar 

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

    Google Scholar 

  • Collins MD, Dixon AFG (1986) The effect of egg depletion on the foraging behaviour of an aphid parasitoid. J Appl Entomol 102:342–352

    Google Scholar 

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

  • Darrouzet E, Huignard J, Chevrier C (2002) Effect of differential host exposure on reproduction in the solitary ectoparasitoid Eupelmus vuilleti. Entomol Exp Appl 103:73–81

    Google Scholar 

  • Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Boulétreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252

    CAS  PubMed  Google Scholar 

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

  • Ellers J (1996) Fat and eggs: an alternative method to measure the trade-offs between survival and reproduction in insect parasitoids. Neth J Zool 46:227–235

    Google Scholar 

  • Ellers J, Jervis MA (2003) Body size and the timing of egg production. Oikos 102:164–172

    Article  Google Scholar 

  • Ellers J, van Alphen JJM, Sevenster JG (1998) A field study of size-fitness relationships in the parasitoid Asobara tabida. J Anim Ecol 67:318–324

    Article  Google Scholar 

  • Flanagan KE, West SA, Godfray HCJ (1998) Local mate competition, variable fecundity and information use in a parasitoid. Anim Behav 56:191–198

    PubMed  Google Scholar 

  • Fletcher JP, Hughes JP, Harvey IF (1994) Life expectancy and egg load affect oviposition decisions of a solitary parasitoid. Proc R Soc Lond B 258:163–167

    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

  • Hanski I (1981) Coexistence of competition in patchy environment with and without predation. Oikos 37:306–312

    Google Scholar 

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

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

    Article  Google Scholar 

  • Hawkins BA (1994) Pattern and process in host–parasitoid interactions. Cambridge University Press: Cambridge

    Google Scholar 

  • Ives AR (1988) Covariance, coexistence and the population-dynamic of 2 competitors using a patchy resources. J Theor Biol 133:345–361

    Google Scholar 

  • Ives AR (1989) The optimal clutch size of insects when many female oviposit per patch. Am Nat 133:671–687

    Article  Google Scholar 

  • Iwasa Y, Suzuki Y, Matsuta H (1984) Theory of oviposition strategy of parasitoids. I. Effect of mortality and limited egg number. Theor Popul Biol 26:205–227

    CAS  PubMed  Google Scholar 

  • Mangel M (1987) Oviposition site selection and clutch size in insects. J Math Biol 25:1–22

    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 

  • Martel V, Boivin G (2004) Impact of competition on sex allocation by Trichogramma. Entomol Exp et Appl 111:29–35

    Article  Google Scholar 

  • Masurier AD le (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 

  • Mayhew PJ (1998a) The evolution of gregariousness in parasitoid wasps. Proc R Soc Lond 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, Glaizot O (2001) Integrating the theory of clutch size and body size evolution for parasitoids. Oikos 92:372–376

    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 

  • Michaud J-P, Mackauer M (1995) Oviposition behaviour of Monoctonus paulensis (Hymenoptera: Aphidiidae): factors influencing reproductive allocation to hosts and host patches. Ann Entomol Soc Am 88:220–226

    Google Scholar 

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

  • 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 

  • Olsen DM, Fadamiro H, Lundgren JG, Heimpel GE (2000) Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol Entomol 25:17–26

    Article  Google Scholar 

  • Parker GA, Courtney SP (1984) Models of clutch size in insect oviposition. Theor Popul Biol 26:27–48

    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, Mayhew PJ (2002) Siblicide and life-history evolution in parasitoids. Behav Ecol 13:690–695

    Article  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

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

    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 

  • Roitberg BD, Sircom J, Roitberg CA, van Alphen JJM, Mangel M (1993) Life expectancy and reproduction. Nature 364:108

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rosenheim JA, Hongkham D (1996) Clutch size in an obligately siblicidal parasitoid wasps. Anim Behav 51:841–852.

    Article  Google Scholar 

  • Rosenheim JA, Rosen D (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of of egg load and experience. J Anim Ecol 60:873–893

    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

  • Shorrocks B, Rosewell J (1987) Spatial patchiness and community structure: coexistence and guild size of drosophilids on ephemeral resources. In: Gee JHR, Giller PS (eds) Organization of communities: past and present. Blackwell, Oxford, pp 29–52

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

    Article  Google Scholar 

  • Smith RH (1991) Genetic and phenotypic aspects of life-history evolution in animals. Adv Ecol Res 21:63–120

    Google Scholar 

  • Stockley P, Parker GA (2002) Life history consequences of mammal sibling rivalry. Proc Natl Acad Sci 99:12932–12937

    Article  Google Scholar 

  • Stokkebo S, Hardy ICW (2000) The importance of being gravid: egg load and contest competition in a parasitoid wasp. Anim Behav 59:1111–1118

    PubMed  Google Scholar 

  • Svensson E, Sheldon BC (1998) The social context of life history evolution. Oikos 83:466–477

    Google Scholar 

  • Turlings TCJ, van Batenberg FHD, van Strien-van Liempt WTFH (1985) Why there is no interspecific host discrimination in the two coexisting larval parasitoids of Drosophila species, Leptopilina heterotoma (Thomson) and Asobara tabida (Nees). Oecologia 67:352–359

    Google Scholar 

  • Vet LEM, Meyer M, Bakker K, van Alphen JJM (1984) Intra- and interspecific host discrimination in Asobara (Hymenoptera) larval endoparasitoids of Drosophilidae: comparison between closely related and less closely related species. Anim Behav 32:871–874

    Google Scholar 

  • Visser ME (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J Anim Ecol 63:963–978

    Google Scholar 

  • Visser ME (1996) The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble competition. Behav Ecol 7:109–114

    Google Scholar 

  • Visser ME, Rosenheim JA (1998) The influence of competition between foragers on clutch size decisions in insect parasitoids. Biol Control 11:169–174

    Article  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

  • Weisser WW, Houston AI (1993) Host discrimination in parasitic wasps: when is it advantagous? Funct Ecol 7:27–39

    Google Scholar 

  • West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688

    CAS  PubMed  Google Scholar 

  • West SA, Flanagan KE, Godfray HCJ (1996) The relationship between parasitoid size and fitness in the field, a study of Achrysocharoides zwoelferi (Hymenoptera: Eulophidae). J Anim Ecol 65:631–639

    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 Calif Publ Entomol 88:1–112

    Google Scholar 

  • Wharton RA (1984) Biology of the Alysiini (Hymenoptera, Braconidae), parasitoids of cyclorrhaphous Diptera. Tech Mono Texas Agr Exp Station 11:1–39

    Google Scholar 

  • Whistlecraft JW, Harris CR, Tomlin AD, Tolman JH (1984) Mass rearing technique for a braconid parasite, Aphaereta pallipes (Say) (Hymenoptera: Braconidae). J Econ Entomol 77:814–816

    Google Scholar 

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

    Google Scholar 

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Acknowledgements

J.J.P. was funded by a NERC studentship. The authors also warmly thank Jeremy Searle, Stu West and three anonymous referees for constructive comments on a previous version of the manuscript. All experiments reported in this study conform to the applicable laws of the United Kingdom.

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  1. John J. Pexton

    Present address: Department of Entomology, North Dakota State University, 202 Hultz Hall, 1300 Albrecht Blvd., Fargo, ND 58105–5346, USA

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

    John J. Pexton & Peter J. Mayhew

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Correspondence to Peter J. Mayhew.

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Communicated by M. Elgar

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Pexton, J.J., Mayhew, P.J. Clutch size adjustment, information use and the evolution of gregarious development in parasitoid wasps. Behav Ecol Sociobiol 58, 99–110 (2005). https://doi.org/10.1007/s00265-004-0881-7

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