Skip to main content

Advertisement

SpringerLink
Log in

Intraspecific hybridization, life history strategies and potential invasion success in a parasitoid wasp

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

Abstract

Classical biological control—the introduction of exotic species to permanently control pests—offers an applied framework to test ecological and evolutionary hypotheses derived from invasion biology. One such hypothesis is that intraspecific hybridization can facilitate invasions because hybrids express higher phenotypic mean and/or variance than their parents. We tested this hypothesis using the parasitoid wasp Psyttalia lounsburyi, a candidate biocontrol agent for the olive fly Bactrocera oleae. Under laboratory conditions, we found marked differentiations between two populations of wasps, from South Africa and Kenya, in terms of life history strategies. South African females were better reproducers than Kenyan females, but the opposite was observed for males. Reaction norms showed different effects of developmental temperature on fecundity depending on the genotype. However, neither heterosis nor hybrid breakdown were observed. Hence, in this system, sex-specific effects of hybridization and genotype-by-environment interactions jeopardize any straightforward prediction on the fitness of hybrids. Therefore, our paper contributes to tone down the hybrid advantage hypothesis in invasion biology.

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
Fig. 5

Similar content being viewed by others

References

  • Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388

    Article  Google Scholar 

  • Antolin MF (1999) A genetic perspective on mating systems and sex ratios of parasitoid wasps. Res Popul Ecol 41:29–37

    Article  Google Scholar 

  • Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10:67–71

    Article  PubMed  CAS  Google Scholar 

  • Arnold ML, Martin NH (2010) Hybrid fitness across time and habitats. Trends Ecol Evol 25:530–536

    Article  PubMed  Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568

    Article  PubMed  CAS  Google Scholar 

  • Bon MC, Jones W, Hurard C, Loiseau A, Ris N, Pickett C, Estoup A, Fauvergue X (2008) Identification of 21 polymorphic microsatellites in the African parasitoid wasp, Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae). Mol Ecol Resour 8:930–932

    Article  PubMed  CAS  Google Scholar 

  • Bordenstein SR, Werren JH (2007) Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia. Heredity 99:278–287

    Article  PubMed  CAS  Google Scholar 

  • Bordenstein SR, O’Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409:707–710

    Article  PubMed  CAS  Google Scholar 

  • Bousset L, Henry PY, Sourrouille P, Jarne P (2004) Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demography. Mol Ecol 13:2023–2036

    Article  PubMed  CAS  Google Scholar 

  • Breeuwer JAJ, Werren JH (1995) Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes. Evolution 49:705–717

    Article  Google Scholar 

  • Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52

    Article  PubMed  CAS  Google Scholar 

  • Campbell DR, Waser NM (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676

    Article  PubMed  CAS  Google Scholar 

  • Cheyppe-Buchmann S, Bon MC, Warot S, Walker J, Malausa T, Fauvergue X, Ris N (2011) Molecular characterization Psyttalia lounsburyi, a candidate biocontrol agent of the olive fly, and its Wolbachia symbionts as a pre-requisite for future intraspecific hybridization. Biocontrol 56:713–724

    Article  Google Scholar 

  • Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    Article  PubMed  CAS  Google Scholar 

  • Connallon T, Knowles LL (2006) Evidence for overdominant selection maintaining X-linked fitness variation in Drosophila melanogaster. Evolution 60:1445–1453

    PubMed  Google Scholar 

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

    Google Scholar 

  • Culley TM, Hardiman NA (2009) The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biol Invasions 11:1107–1119

    Article  Google Scholar 

  • Daane KM, Sime KR, Wang XG, Nadel H, Johnson MW, Walton VM, Kirk A, Pickett CH (2008) Psyttalia lounsburyi (Hymenoptera: Braconidae), potential biological control agent for the olive fruit fly in California. Biol Control 44:79–89

    Article  Google Scholar 

  • Dowling DK, Abiega KC, Arnqvist G (2007) Temperature-specific outcomes of cytoplasmic-nuclear interactions on egg-to-adult development time in seed beetles. Evolution 61:194–201

    Article  PubMed  Google Scholar 

  • Dowling DK, Friberg U, Lindell J (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol Evol 23:546–554

    Article  PubMed  Google Scholar 

  • Edmands S (2002) Does parental divergence predict reproductive compatibility? Trends Ecol Evol 17:520–527

    Article  Google Scholar 

  • Ehler LE (1998) Invasion biology and biological control. Biol Control 13:127–133

    Article  Google Scholar 

  • Ellison CK, Burton RS (2010) Cytonuclear conflict in interpopulation hybrids: the role of RNA polymerase in mtDNA transcription and replication. J Evol Biol 23:528–538

    Article  PubMed  CAS  Google Scholar 

  • Ellison CK, Niehuis O, Gadau J (2008) Hybrid breakdown and mitochondrial dysfunction in hybrids of Nasonia parasitoid wasps. J Evol Biol 21:1844–1851

    Article  PubMed  CAS  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535

    Article  PubMed  CAS  Google Scholar 

  • Facon B, Pointier JP, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367

    Article  PubMed  CAS  Google Scholar 

  • Fagan WF, Lewis MA, Neubert MG, van den Driessche P (2002) Invasion theory and biological control. Ecol Lett 5:148–157

    Article  Google Scholar 

  • Fauvergue X, Hopper KR (2009) French wasps in the new world: experimental biological control introductions reveal a demographic Allee effect. Popul Ecol 51:385–397

    Article  Google Scholar 

  • Fauvergue X, Malausa JC, Giuge L, Courchamp F (2007) Invading parasitoids suffer no Allee effect: a manipulative field experiment. Ecology 88:2392–2403

    Article  PubMed  Google Scholar 

  • Frankham R (2005) Invasion biology—resolving the genetic paradox in invasive species. Heredity 94:385

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Grevstad FS (1999) Experimental invasions using biological control introductions: the influence of release size on the chance of population establishment. Biol Invasions 1:313–323

    Article  Google Scholar 

  • Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW, Parker JD (1997) Evolutionary genetics and genetic variation of haplodiploids and X-linked genes. Annu Rev Ecol Syst 28:55–83

    Article  Google Scholar 

  • Holm S (1979) A simple sequential rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Hufbauer RA (2008) Biological invasions: paradox lost and paradise gained. Curr Biol 18:R246–R247

    Article  PubMed  CAS  Google Scholar 

  • Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns, and processes. Biol Control 35:227–239

    Article  Google Scholar 

  • Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: Hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60:1585–1595

    PubMed  CAS  Google Scholar 

  • Keller SR, Taylor DR (2010) Genomic admixture increases fitness during a biological invasion. J Evol Biol 23:1720–1731

    Article  PubMed  CAS  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236

    Article  PubMed  CAS  Google Scholar 

  • Kolbe JJ, Glor RE, Rodríguez Schettino L, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  PubMed  CAS  Google Scholar 

  • Krackow S, Meelis E, Hardy ICW (2002) Analysis of sex ratio variances and sequences of sex allocations. In: Hardy ICW (ed) Sex ratios—concepts and research methods. Cambridge University Press, Cambridge, pp 112–131

    Chapter  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • Legner EF (1988) Quantitation of heterotic behavior in parasitic Hymenoptera. Ann Entomol Soc Am 81:657–681

    Google Scholar 

  • Lexer C, Randell RA, Rieseberg LH (2003) Experimental hybridization as a tool for studying selection in the wild. Ecology 84:1688–1699

    Article  Google Scholar 

  • Lowe A, Harris S, Ashton P (2004) Ecological genetics: design, analysis and application. Blackwell, Oxford

    Google Scholar 

  • Malausa J-C, Blanchet A, Bon MC, Cheyppe-Buchmann S, Groussier-Bout G, Jones W, Pickett C, Ris N, Roche M, Thaon M, Fauvergue X (2010) Introduction of the African parasitoid Psyttalia lounsburyi in south of France for the classical biological control of Bactrocera oleae: will hybridization affect establishment and population growth? IOBC/WPRS Bull 53:49–55

    Google Scholar 

  • Marchetti MP, Moyle PB, Levine R (2004) Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol Appl 14:587–596

    Article  Google Scholar 

  • Marsico TD, Burt JW, Espeland EK, Gilchrist GW, Jamieson MA, Lindstrom L, Roderick GK, Swope S, Szucs M, Tsutsui ND (2010) Underutilized resources for studying the evolution of invasive species during their introduction, establishment, and lag phases. Evol Appl 3:203–219

    Article  Google Scholar 

  • Memmott J, Craze PG, Harman HM, Syrett P, Fowler SV (2005) The effect of propagule size on the invasion of an alien insect. J Anim Ecol 74:50–62

    Article  Google Scholar 

  • Montgomery DC, Peck EA, Vining GG (2001) Introduction to linear regression analysis, 3rd edn. Wiley, New York

    Google Scholar 

  • Niehuis O, Judson AK, Gadau J (2008) Cytonuclear genic incompatibilities cause increased mortality in male F-2 hybrids of Nasonia giraulti and N. vitripennis. Genetics 178:413–426

    Article  PubMed  CAS  Google Scholar 

  • Niehuis O, Gibson JD, Rosenberg MS, Pannebakker BA, Koevoets T, Judson AK, Desjardins CA, Kennedy K, Duggan D, Beukeboom LW, van de Zande L, Shuker DM, Werren JH, Gadau J (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5(1):e8597

    Article  PubMed  Google Scholar 

  • O’Brien RG (1979) A general ANOVA method for robust tests of additive models for variances. J Am Stat Assoc 74:877–881

    Article  Google Scholar 

  • O’Brien RG (1981) A simple test for variance effects in experimental designs. Psychol Bull 89:570–574

    Article  Google Scholar 

  • Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721

    Article  Google Scholar 

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

    Google Scholar 

  • Rand DM, Haney RA, Fry AJ (2004) Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 19:645–653

    Article  PubMed  Google Scholar 

  • Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372

    Article  PubMed  Google Scholar 

  • Ris N, Allemand R, Fouillet P, Fleury F (2004) The joint effect of temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of Drosophila, Leptopilina heterotoma (Hymenoptera: Figitidae). Oikos 106:451–456

    Article  Google Scholar 

  • Roff D (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York

    Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B-Biol Sci 273:2453–2459

    Article  Google Scholar 

  • Rosenthal DM, Ramakrishnan AP, Cruzan MB (2008) Evidence for multiple sources of invasion and intraspecific hybridization in Brachypodium sylvaticum (Hudson) Beauv. in North America. Mol Ecol 17:4657–4669

    Article  PubMed  Google Scholar 

  • Rugman-Jones PF, Wharton R, van Noort T, Stouthamer R (2009) Molecular differentiation of the Psyttalia concolor (Szepligeti) species complex (Hymenoptera: Braconidae) associated with olive fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), in Africa. Biol Control 49:17–26

    Article  CAS  Google Scholar 

  • SAS Institute Inc. (1999) SAS/Stat User’s Guide, Version 9.1.3. SAS Institute, Cary, North Carolina.

  • Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371

    Article  Google Scholar 

  • Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions 11:1093–1105

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stebbins GL (1959) The role of hybridization in evolution. Proc Am Phil Soc 103:231–251

    Google Scholar 

  • Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM (2008) Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol 8:33. doi:10.1186/1471-2229-8-33

    Article  PubMed  Google Scholar 

  • Thaon M, Blanchet A, Ris N (2009) Contribution à l’optimisation de l’élevage du parasitoïde Psyttalia lounsburyi. Cah Techn Inra 66:21–31

    Google Scholar 

  • Verhoeven KJF, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc R Soc B-Biol Sci 278:2–8

    Article  Google Scholar 

  • Wolfe LM, Blair AC, Penna BM (2007) Does intraspecific hybridization contribute to the evolution of invasiveness?: an experimental test. Biol Invasions 9:515–521

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Benoît Facon, Thomas Guillemaud, and Ruth Hufbauer for helpful comments on the manuscript as well as Marcel Thaon for providing biological material. This study was partially funded by the Agence Nationale de la Recherche (project BioInv4I, ANR-06-BDIV-008-01).

Author information

Author notes

  1. Chiara Benvenuto

    Present address: UCD School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

Authors and Affiliations

  1. Biology of Introduced Populations, Institute Sophia-Agrobiotech, (INRA–CNRS–UNS), Sophia-Antipolis, France

    Chiara Benvenuto, Sandrine Cheyppe-Buchmann & Xavier Fauvergue

  2. Research and Development in Biological Control, Institute Sophia-Agrobiotech, (INRA–CNRS–UNS), Sophia-Antipolis, France

    Gérald Bermond & Nicolas Ris

  3. Research and Development in Biological Control, Centre INRA PACA, 400 route des Chappes, BP 167, 06903, Sophia-Antipolis, France

    Nicolas Ris

Authors
  1. Chiara Benvenuto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandrine Cheyppe-Buchmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gérald Bermond
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Ris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xavier Fauvergue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicolas Ris.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benvenuto, C., Cheyppe-Buchmann, S., Bermond, G. et al. Intraspecific hybridization, life history strategies and potential invasion success in a parasitoid wasp. Evol Ecol 26, 1311–1329 (2012). https://doi.org/10.1007/s10682-011-9553-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9553-z

Keywords

Search

Navigation