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A Comparative Study of Sex Ratio and Clutch Size in Gregarious Ichneumonoid Wasps

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Abstract

Some convincing support for sex ratio theory comes from the cross-species relationship between sex ratio and brood size in gregarious bethylid wasps (Hymenoptera: Bethylidae), in which the proportion males declines as brood size increases as predicted under local mate competition. It is unknown how widely such relationships hold within parasitoid wasps as a whole. We assemble a dataset on sex ratio and brood size for gregarious Braconidae and Ichneumonidae. Their sex ratios deviate substantially from those of bethylids; sex ratios differ widely across species; and they are not significantly related to brood size across species. Several factors explain the heterogeneity in sex ratios including across-species differences in mating system, sex determining mechanism, and sexual asymmetries in larval competition and polyembryony leading to single-sexed broods.

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References

  • Abbas MST, Abou-Zeid NA (1983) Biological studies on Bracon instabilis Marsh. (Hym., Braconidae), a larval parasite of Phthorimaea operculella Zell. (Lep., Gelechiidae) in Egypt. Z Angew Entomol 96:32–36

    Google Scholar 

  • Alford DV (1968) The biology and immature stages of Syntretus splendidus (Marshall) (Hymenoptera: Braconidae, Euphorinae). Trans Roy Entomol Soc Lond 120:375–393

    Google Scholar 

  • Antolin MF, Strand MR (1992) Mating system of Bracon hebetor (Hymenoptera: Braconidae). Ecol Entomol 17:1–7

    Article  Google Scholar 

  • Antolin MF, Ode PJ, Strand MR (1995) Variable sex ratios and ovicide in an outbreeding parasitic wasp. Anim Behav 49:589–600

    Google Scholar 

  • Azab AK, Twafk MFS, Nagui A (1969) Studies on the biology of Microbracon kirkpatricki Wilk. in Egypt. Bull Soc Entomol Egypte 52:251–271

    Google Scholar 

  • Batchelor TP, Hardy ICW, Barrera JF, Pérez-Lachaud G (2005) Insect gladiators II: competitive interactions within and between bethylid parasitoid species of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Biol Control 33:194–202

    Article  Google Scholar 

  • Belshaw R, Grafen A, Quicke DLJ (2003) Inferring life history from ovipositor morphology wasps using phylogenetic regression and discriminant analysis. Zool J Linn Soc 139:213–228

    Article  Google Scholar 

  • Benjamin DM, Demba NM (1968) Notes on the biologies of three parasites of the eggs of Entypotrachelus meyeri Kolbe and E.micans Hust. (Col., Curculionidae) laid on tea and Cinchona. Bull ent Res 59:473–478

    Google Scholar 

  • Bennett FD (1960) Parasites of Ancylostoma stercorea (Zell.) (Pyralidae, Lepidoptera), a pod borer attacking pigeon pea in Trinidad. Bull ent Res 50:737–757

    Google Scholar 

  • Bernal JS, Gillogly PO, Griset J (2001) Family planning in a stemborer parasitoid: sex ratio, brood size and size–fitness relationships in Parallorhogas pyralophagus (Hymenoptera: Braconidae) and implications for biological control. Bull Ent Res 91:255–264

    CAS  Google Scholar 

  • Bryan DE, Jackson CG, Patana R, Neeman EG (1971) Field cage laboratory studies with Bracon kirkpatricki, a parasite of the pink bollworm. J Econ Entomol 64:1236–1241

    Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton Univ. Press, Princeton

    Google Scholar 

  • Charnov EL (1993) Life history invariants. Oxford Univ. Press, Oxford

    Google Scholar 

  • Charnov EL, los-den Hartogh RL, Jones WT, van den Assem J (1981) Sex ratio evolution in a variable environment. Nature 289:27–33

    Article  PubMed  CAS  Google Scholar 

  • Clausen CP (1940) Entomophagous insects. McGraw Hill, New York

    Google Scholar 

  • Cook JM (1993a) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

  • Cook JM (1993b) Experimental tests of sex determination in Goniozus nephantidis (Hymenoptera: Bethylidae). Heredity 71:130–137

    Article  Google Scholar 

  • Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286

    Article  Google Scholar 

  • Cook JM, Rivero Lynch AP, Godfray HCJ (1994) Sex ratio and foundress number in the parasitoid wasp Bracon hebetor. Anim Behav 47(3):687–696

    Article  Google Scholar 

  • Cross WH, McGovern WL, Mitchell HC (1969) Biology of Bracon kirkpatricki and field releases of the parasite control of the Boll Weevil. J Econ Entomol 62:448–454

    Google Scholar 

  • De Boer JG, Ode PJ, Vet LEM, Whitfield JB, Heimpel GE (2007) Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. Heredity 99:288–294

    Article  PubMed  Google Scholar 

  • De Boer JG, Ode PJ, Rendahl AK, Vet LEM, Whitfield JB, Heimpel GE (2008) Experimental support for multiple locus complementary sex determination in the parasitoid Cotesia vestalis. Genetics 180:1525–1535

    Article  PubMed  Google Scholar 

  • Dorn S, Beckage NE (2007) Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiol Entomol 32:199–211

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fox CW, Roff DA, Fairbairn DJ (2001) Evolutionary ecology: concepts and case studies. Oxford Univ. Press, New York

    Google Scholar 

  • Fuester RW, Swan KS, Dunning K, Taylor PB, Ramaseshiah G (2003) Male-biased sex ratios in Glyptapanteles flavicoxis (Hymenoptera: Braconidae), a parasitoid of the gypsy moth (Lepidoptera: Lymantriidae). Ann Entomol Soc Am 96:553–559

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Gauld I, Bolton B (eds) (1988) The Hymenoptera. Oxford Univ. Press, Oxford

  • Gifford JR, Mann GA (1967) Biology, rearing, and trial release of Apanteles flavipes in the Florida everglades to control the sugarcane borer. J Econ Entomol 60:44–47

    Google Scholar 

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

    Google Scholar 

  • Goubault M, Scott D, Hardy ICW (2007) The importance of offspring value: maternal defence in parasitoid contests. Anim Behav 74:437–446

    Article  Google Scholar 

  • Griffiths NT, Godfray HCJ (1988) Local mate competition, sex ratio and clutch size in bethylid wasps. Behav Ecol Sociobiol 22:211–217

    Article  Google Scholar 

  • Guertin DS, Ode PJ, Strand MR, Antolin MF (1996) Host-searching and mating in an outbreeding parasitoid wasp. Ecol Entomol 21:27–33

    Article  Google Scholar 

  • Hafez M (1947) The biology and life-history of Apanteles ruficrus Hal. (Hymenoptera- Braconidae). Bull Soc Fouad 1 Ent 31:225–249

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hardy ICW (1992) Non-binomial sex allocation and brood sex ratio variances in the parasitoid Hymenoptera. Oikos 65:143–158

    Article  Google Scholar 

  • Hardy ICW (1994) Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos 69:3–20

    Article  Google Scholar 

  • Hardy ICW (ed) (2002) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge

  • Hardy ICW, Blackburn TM (1991) Brood guarding in a bethylid wasp. Ecol Entomol 16:55–62

    Article  Google Scholar 

  • Hardy ICW, Mayhew PJ (1998a) Sex ratio, sexual dimorphism and mating structure in bethylid wasps. Behav Ecol Sociobiol 42:383–395

    Article  Google Scholar 

  • Hardy ICW, Mayhew PJ (1998b) Partial local mating and the sex ratio: indirect comparative evidence. Trends Ecol Evol 13:431–432

    Article  Google Scholar 

  • Hardy ICW, Dijkstra LJ, Gillis JEM, Luft PA (1998) Patterns of sex ratio, virginity and developmental mortality in gregarious parasitoids. Biol J Linn Soc 64:239–270

    Article  Google Scholar 

  • Hardy ICW, Pedersen JB, Sejr MK, Linderoth UH (1999) Local mating, dispersal, and sex ratio in a gregarious parasitoid wasp. Ethology 105:57–72

    Google Scholar 

  • Hardy ICW, Stokkebo S, Bønløkke-Pedersen J, Sejr MK (2000) Insemination capacity and dispersal in relation to sex allocation decisions in Goniozus legneri (Hymenoptera: Bethylidae): why are there more males in larger broods? Ethology 106:1021–1032

    Article  Google Scholar 

  • Hardy ICW, Ode PJ, Siva-Jothy MT (2005) Mating systems. In: Jervis M (ed) Insects and natural enemies: a practical perspective. Springer, Dordrecht, pp 261–298

    Chapter  Google Scholar 

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

    Google Scholar 

  • Hawkins BA, Smith JW Jr (1986) Rhaconotus roslinensis (Hymenoptera: Braconidae), a candidate for biological control of stalkboring sugarcane pests (Lepidotera: Pyralidae): Development, life tables, and intraspecific competition. Ann Entomol Soc Am 79:905–911

    Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230

    Article  PubMed  CAS  Google Scholar 

  • Herre EA (1985) Sex ratio adjustment in fig wasps. Science 228:896–898

    Article  PubMed  Google Scholar 

  • Holdaway FT, Smith HF (1933) A relationship between the size of host puparia and sex ratio of Alysia manducator. Aust J Expt Biol Med Sci 10:247–259

    Article  Google Scholar 

  • Holloway AK, Strand MR, Black WC IV, Antolin MF (2000) Linkage analysis of sex determination in Bracon sp. nr hebetor (Hymenoptera: Braconidae). Genetics 154:205–212

    PubMed  CAS  Google Scholar 

  • King BH (1987) Offspring–sex ratios in parasitic wasps. Quart Rev Biol 64:367–396

    Google Scholar 

  • Kitano H (1976) Studies on the courtship behaviour of Apanteles glomeratus L. 3. On the behaviour of a males and females after their emergence from cocoons. Jap J Physiol Ecol 17:383–393

    Google Scholar 

  • Laing DR, Caltairone LE (1969) Biology of Habrobracon lineatellae (Hymenoptera: Braconidae). Can Entomol 101:135–142

    Google Scholar 

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

    Article  Google Scholar 

  • Li SY, Fitzpatrick SM, Ttroubridge JT, Sharkey MJ, Barron JR, O'Hara JE (1999) Parasitoids reared from the oblique banded leafroller (Lepidoptera: Tortricidae) infesting raspberries. Can Entomol 131:399–404

    Article  Google Scholar 

  • MacArthur RH (1972) Geographical ecology. Princeton Univ. Press, Princeton

    Google Scholar 

  • Mayhew PJ (1997) Fitness consequences of ovicide in a parasitoid wasp. Entmol Exp et Appl 84:115–126

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Mayhew PJ (2006) Discovering evolutionary ecology: bringing together ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Mayhew PJ, Godfray HCJ (1997) Mixed sex allocation strategies in a parasitoid wasp. Oecologia 110:218–221

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mayhew PJ, Heitmans WRB (2000) Life history correlates and reproductive biology of Laelius pedatus (Hymenoptera: Bethylidae) in The Netherlands. Eur J Entomol 97:313–322

    Google Scholar 

  • Mayhew PJ, Pen I (2002) Comparative analysis of sex ratios. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 132–156

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Nagelkerke CJ, Hardy ICW (1994) The influence of developmental mortality on optimal sex allocation under local mate competition. Behav Ecol 5:401–411

    Article  Google Scholar 

  • Narayanan ES, Subba Rao BR (1995) Studies in insect parasitism I–III. Beit Entomol 5:36–60

    Google Scholar 

  • Niyibigira EI, Overholt WA, Stouthamer R (2004) Cotesia flavipes Cameron and Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) do not exhibit complementary sex determination: evidence from field populations. Appl Entomol Zool 39:705–715

    Article  Google Scholar 

  • Nunney L, Luck RF (1988) Factors influencing the optimum sex ratio in a structured population. Theor Pop Biol 33:1–30

    Article  CAS  Google Scholar 

  • Ode PJ, Hardy ICW (2008) Parasitoid sex ratios and biological control. In: Wajnberg E, Bernstein C, van Alphen JJM (eds) Behavioural ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell, Oxford, pp 253–291

    Chapter  Google Scholar 

  • Ode PJ, Antolin MF, Strand MR (1995) Brood-mate avoidance in the parasitic wasp Bracon hebetor Say. Anim Behav 49:1239–1248

    Article  Google Scholar 

  • Ode PJ, Antolin MJ, Strand MR (1998) Differential dispersal and female biased sex allocation in a parasitic wasp. Ecol Entomol 23:314–318

    Article  Google Scholar 

  • Olaifa JI, Akingbohungbe AE (1982) Bionomics of Bracon ?hancocki (Wilkinson) (Hymenoptera: Braconidae), a larval parasite of Cydia ptychora (Meyrick) (Lepidoptera: Tortricidae) in Nigeria. Bull Ent Res 72:567–572

    Google Scholar 

  • Pexton JJ, Mayhew PJ (2004) Competitive interactions between parasitoid larvae and the evolution of gregarious development. Oecologia 141:179–190

    Article  PubMed  Google Scholar 

  • Pexton JJ, Mayhew PJ (2005) Clutch size adjustment, information use and the evolution of gregarious development in parasitoid wasps. Behav Ecol Sociobiol 58:99–110

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pickering J (1980) Larval competition and brood sex ratios in the gregarious parasitoid Pachysomoides stupidus. Nature 283:291–292

    Article  Google Scholar 

  • Pramanik LM, Choudhury MK (1963) Effect of superparasitism on the development, sex ratio and progeny of Bracon greeni Ashmead. Entomophaga 8:83–86

    Article  Google Scholar 

  • Price T (1997) Correlated evolution and independent contrasts. Phil Trans Roy Soc Lond B 352:519–529

    Article  CAS  Google Scholar 

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comp Appl Biosci 11:247–251

    PubMed  CAS  Google Scholar 

  • Purvis A, Gittleman JL, Luh HK (1994) Truth or consequences: effects of phylogenetic accuracy on two comparative methods. J Theor Biol 167:293–300

    Article  Google Scholar 

  • Salt G (1931) Parasites of the wheat-stem sawfly, Cephus pygmaeus, Linnaeus, in England. Bull Ent Res 22:479–545

    Article  Google Scholar 

  • Shaw MR (1995) Observations on the adult behaviour and biology of Histeromerus mystacinus Wesmael (Hymenoptera: Braconidae). Entomologist 114:1–13

    Google Scholar 

  • Shaw MR (2002) A new species of Macrostomion Szepligeti (Hymenoptera: Braconidae: Rogadinae) from Papua New Guinea, with notes on the biology of the genus. Zool Meded 76:133–140

    Google Scholar 

  • Shaw MR, Huddleston T (1991) Classification and biology of braconid wasps: handbooks for the identification of British insects. Royal entomological society of London, 7: Part 11. Henry Ling Ltd, London

    Google Scholar 

  • Strand MR, Godfray HCJ (1989) Superparasitism and ovicide in parasitic Hymenoptera: theory and a case study of the ectoparasitoid Bracon hebetor. Behav Ecol Sociobiol 24:421–432

    Article  Google Scholar 

  • Tagawa J (2000) Sex allocation and clutch size in the gregarious larval endoparasitoid wasp, Cotesia glomerata. Entomol Exp et Appl 97:193–202

    Article  Google Scholar 

  • Takasu K, Overholt WA (1998) Brood guarding behavior and life histroy characteristics of Goniozus indicus Ashmead (Hymenoptera: Bethylidae), a larval ectoparasitoid of lepidopteran stemborers. Appl Entomol Zool 33:121–126

    Google Scholar 

  • Traynor (2004) Life history evolution in the parasitoid Hymenoptera. PhD Thesis University of York, UK

  • Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    Article  PubMed  CAS  Google Scholar 

  • 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 den Assem J, van Iersel JJA, los-den Los-Hartogh RL (1989) Is being large more important for female than for male parasitic wasps? Behaviour 108:160–195

    Article  Google Scholar 

  • van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1–15

    Article  PubMed  CAS  Google Scholar 

  • Vet LEM, Datema A, Janssen A, Snellen H (1994) Clutch size in a larval–pupal endoparasitoid: consequences for fitness. J Anim Ecol 63:807–815

    Article  Google Scholar 

  • Waloff N (1961) Observations on the biology of Perilitus dubius (Wesmael) (Hymenoptera: Braconidae), a parasite of the chrysomelid beetle Phytodecta olivacea (Forster). Proc Roy Entomol Soc Lond A 36:96–102

    Google Scholar 

  • Werren JH (1983) Sex ratio evolution under local mate competition in a parasitic wasp. Evolution 37:116–124

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 48–92

    Google Scholar 

  • Zaldivar-Riverón A, Mori M, Quicke DLJ (2006) Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): a simultaneous molecular and morphological Bayesian approach. Mol Phyl Evol 38:130–145

    Article  CAS  Google Scholar 

  • Zhou Y, Gu H, Dorn S (2006) Single-locus sex determination in the parasitoid wasp Cotesia glomerata (Hymenoptera: Braconidae). Heredity 96:487–492

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Gu H, Dorn S (2007) Effects of inbreeding on fitness components of Cotesia glomerata, a parasitoid wasp with single-locus complementary sex determination (sl-CSD). Biol Control 40:273–279

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the many authors who sent us papers and references for this study, and Ian Hardy and an anonymous referee for comments. This research complies with UK law.

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

    Christina B. Smart & Peter J. Mayhew

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  1. Christina B. Smart
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Correspondence to Peter J. Mayhew.

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Smart, C.B., Mayhew, P.J. A Comparative Study of Sex Ratio and Clutch Size in Gregarious Ichneumonoid Wasps. J Insect Behav 22, 273–288 (2009). https://doi.org/10.1007/s10905-008-9172-x

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