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Species differences in bumblebee immune response predict developmental success of a parasitoid fly

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Abstract

Endoparasitoids develop inside the body of a host organism and, if successful, eventually kill their host in order to reach maturity. Host species can vary in their suitability for a developing endoparasitoid; in particular, the host immune response, which can suppress egg hatching and larval development, has been hypothesized to be one of the most important determinants of parasitoid host range. In this study, we investigated whether three bumblebee host species (Bombus bimaculatus, Bombus griseocollis, and Bombus impatiens) varied in their suitability for the development of a shared parasitoid, the conopid fly (Conopidae, Diptera) and whether the intensity of host encapsulation response, an insect immune defense against invaders, could predict parasitoid success. When surgically implanted with a nylon filament, B. griseocollis exhibited a stronger immune response than both B. impatiens and B. bimaculatus. Similarly, B. griseocollis was more likely to melanize conopid larvae from natural infections and more likely to kill conopids prior to its own death. Our results indicate that variation in the strength of the general immune response of insects may have ecological implications for sympatric species that share parasites. We suggest that, in this system, selection for a stronger immune response may be heightened by the pattern of phenological overlap between local host species and the population peak of their most prominent parasitoid.

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References

  • Allander K, Schmid-Hempel P (2000) Immune defense reaction in bumble-bee workers after a previous challenge and parasitic coinfection. Funct Ecol 14:711–717

    Article  Google Scholar 

  • Ameri M, Rasekh A, Michaud JP (2014) Body size affects host defensive behavior and progeny fitness in a parasitoid wasp, Lysiphlebus fabarum. Entomol Exp Appl 150:259–268

    Article  Google Scholar 

  • Ardia DR, Parmentier HK, Vogel LA (2011) The role of constraints and limitation in driving individual variation in immune response. Funct Ecol 25:61–73

    Article  Google Scholar 

  • Ardia DR, Gantz JE, Schneiden BC, Strebel S (2012) Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739

    Article  Google Scholar 

  • Barribeau SM, Schmid-Hempel P (2013) Qualitatively different immune response of the bumblebee host, Bombus terrestris, to infection by different clones of the trypanosome gut parasite, Crithidia bombi. Infect Genet Evol 20:249–256

    Article  CAS  PubMed  Google Scholar 

  • Bartlett BR, Ball JC (1966) The evolution of host suitability in a polyphagous parasite with special reference to the role of parasite egg encapsulation. Ann Entomol Soc Am 59(1):42–45

    Article  Google Scholar 

  • Boots M, Best A, Miller MR, White A (2009) The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philos Trans R Soc Lond B Biol Sci 364:27–36

    Article  PubMed Central  PubMed  Google Scholar 

  • Brodeur J, Vet LEM (1995) Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two relates parasitoid species. Physiol Entomol 20:7–12

    Article  Google Scholar 

  • Brown M, Moret Y, Schmid-Hempel P (2003a) Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parisitology 126:253–260

    Article  CAS  Google Scholar 

  • Brown M, Loosli R, Schmid-Hempel P (2003b) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91(3):421–427

    Article  Google Scholar 

  • Bugila AAA, Franco JC, da Silva EB, Branco M (2014) Defense response of native and alien mealybugs (Hemiptera: Pseudococcidae) against the solitary parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera, Encyrtidae). J Insect Behav 27:439–453

    Google Scholar 

  • Bushmann SL, Drummond FA, Beers LA, Groden E (2012) Wild bumblebee (Bombus) diversity and Nosema (Microsporidia: Nosematidae) infection levels associates with lowbush blueberry (Vaccinium angustifolium) production and commercial bumblebee pollinators. Psyche. doi:10.1155/2012/429398

    Google Scholar 

  • Cameron S (1985) Ethometry of division of labor among workers and males in primitively social bees and wasps (Hymenoptera: Apidae and Vespidae). PhD Dissertation, University of Kansas, Lawrence

  • Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kans Entomol Soc 60:145–147

    Google Scholar 

  • Cartar RV (1992) Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumblebees. J Anim Ecol 61:225–231

    Article  Google Scholar 

  • Carton Y, Poirié M, Nappi AJ (2008) Insect immune resistance to parasitoids. Insect Sci 15:67–87

    Article  CAS  Google Scholar 

  • Chauhan A, Katna S, Rana BS, Sharma HK (2013) Studies on pests and diseases of bumble bee (Bombus haemorrhoidalis Smith) in India. J Med Sci Clin Res 1(2):93–98

    Google Scholar 

  • Desneux N, Blahnik R, Delebecque CJ, Heimpel GE (2012) Host phylogeny and specialisation in parasitoids. Ecol Lett 15:453–460

    Article  PubMed  Google Scholar 

  • Dobson AP, Hudson PJ (1986) Parasites, disease and the structures of ecological communities. Trends Ecol Evol 1:11–14

    Article  CAS  PubMed  Google Scholar 

  • Doums C, Schmid-Hempel P (2000) Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection. Can J Zool 78:1060–1066

    Article  Google Scholar 

  • Feener DH (1981) Competition between ant species: outcome controlled by parasitic flies. Science 214:815–817

    Article  PubMed  Google Scholar 

  • Feener DH, Brown BV (1997) Diptera as parasitoids. Annu Rev Entomol 42:73–97

    Article  CAS  PubMed  Google Scholar 

  • Fors L, Markus R, Theopold U, Hamback PA (2014) Differences in cellular immune response explain parasitoid resistance for two coleopteran species. PLoS One 9(9):e108795. doi:10.1371/journal.pone.0108795

    Article  PubMed Central  PubMed  Google Scholar 

  • Freeman BA (1966) Notes on conopid flies, including insect host, plant and phoretic relationships (Diptera: Conopidae). J Kans Entomol Soc 39:123–131

    Google Scholar 

  • Geervliet JBF, Brodeur J (1992) Host species affecting the performance of the larval parasitoids Cotesia glomerata and Cotesia rubecula (Hymenoptera: Braconidae). II. Comparative suitability of three Pieris species (Lepidoptera: Pieridae). Meded Fac Landbouwwet Rijksuniv Gent 57:546–550

    Google Scholar 

  • Gillespie S (2010) Factors affecting parasite prevalence among wild bumblebees. Ecol Entomol 35:737–747

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids. Princeton University Press, Princeton

    Google Scholar 

  • Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5–17

    Article  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Article  Google Scholar 

  • Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PLoS One. doi:10.1371/journal.pone.0019997

    Google Scholar 

  • Havard S, Pelissier C, Ponsard S, Campan EDM (2014) Suitability of three Ostrinia species as hosts for Macrocentus cingulum: a comparison of their encapsulation abilities. Insect Sci 21:93–102

    Article  PubMed  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Article  Google Scholar 

  • Imhoof B, Schmid-Hempel P (1998) Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117(4):331–336

    Article  PubMed  Google Scholar 

  • Jaenike J, Holt RD (1991) Genetic variation for habitat preference: evidence and explanations. Am Nat 137:S67–S90

    Article  Google Scholar 

  • König C, Schmid-Hempel P (1995) Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proc Biol Sci 260:225–227

    Article  Google Scholar 

  • Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280

    Article  CAS  PubMed  Google Scholar 

  • Kraaijeveld AR, Godfray HCJ (1999) Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am Nat 153(S5):S61–S74

    Article  Google Scholar 

  • Kraaijeveld AR, van der Wel NN (1994) Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species. Ecol Entomol 19:221–229

    Article  Google Scholar 

  • Kraaijeveld AR, Nowee B, Najem RW (1995) Adaptive variation in host selection behavior of Asobara tabida, a parasitoid of Drosophila larvae. Funct Ecol 9:113–118

    Article  Google Scholar 

  • Kraaijeveld AR, van Alphen JJM, Godfray HCJ (1998) The coevolution of host resistance and parasitoid virulence. Parasitology 116:S29–S45

    Article  PubMed  Google Scholar 

  • Lindstrom KM, Foufopoulos J, Parn H, Wilkelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc R Soc B Biol Sci 271:1513–1519

    Article  Google Scholar 

  • Maeta Y, MacFarlane RP (1993) Japanese Conopidae (Diptera): their biology, overall distribution, and role as parasites of bumble bees (Hymenoptera, Apidae). Jpn J Entomol 61:493–509

    Google Scholar 

  • Mahmoud AMA, De Luna-Santillana EJ, Guo X, Rodríguez-Pérez MA (2012) Parasitism by Cotesia flavipes alters the haemocyte population and phenoloxidase activity of the sugarcane borer, Diatraea saccharalis. Can Entomol 144(4):599–608

    Article  Google Scholar 

  • Malfi RL, Roulston TH (2014) Patterns of parasite infection in bumble bees (Bombus spp.) of northern Virginia. Ecol Entomol 39:17–29

    Article  Google Scholar 

  • Malfi RL, Davis SE, Roulston TH (2014) Parasitoid fly induces grave-digging behavior differentially across its bumblebee hosts. Anim Behav 92:213–220

    Article  Google Scholar 

  • Martin LD, Hawley DM, Ardia DR (2011) An introduction to ecological immunity. Funct Ecol 25:1–4

    Article  Google Scholar 

  • McNeill MR, Vittum PJ, Baird DB (1999) Suitability of Listronotus maculicollis (Coleoptera: Curculionidae) as a host for Microctonus hyperodae (Hymenoptera: Braconidae). J Econ Entomol 92(6):1292–1300

    Article  Google Scholar 

  • Michener CD (1974) The social behavior of the bees: a comparative study. Harvard University Press, Cambridge

    Google Scholar 

  • Minchella DJ, Scott ME (1991) Parasitism: a cryptic determinant of animal community structure. Trends Ecol Evol 6:250–254

    Article  CAS  PubMed  Google Scholar 

  • Muller CB (1994) Parasitoid induced digging behavior in bumblebee workers. Anim Behav 48:961–966

    Article  Google Scholar 

  • Muller CB, Schmid-Hempel P (1992) Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecol Entomol 17:343–353

    Article  Google Scholar 

  • Nappi AJ, Christensen BM (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 35:443–459

    Article  CAS  PubMed  Google Scholar 

  • Otterstatter MC (2004) Patterns of parasitism among conopid flies parasitizing bumblebees. Entomol Exp Appl 11:135–139

    Google Scholar 

  • Otterstatter MC, Whidden TL, Owen RE (2002) Contrasting frequencies of parasitism and host mortality among phorid and conopid parasitoids of bumble-bees. Ecol Entomol 27:229–237

    Article  Google Scholar 

  • Pelletier L, McNiel JN (2003) The effect of food supplementation on reproductive success in bumblebee field colonies. Oikois 103:688–694

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1995) “Adaptive” changes in the behavior of parasitized animals: a critical review. Int J Parasitol 25:1371–1383

    Article  CAS  PubMed  Google Scholar 

  • Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus. Funct Ecol 19:323–330

    Article  Google Scholar 

  • Rantala MJ, Roff DA (2007) Inbreeding and extreme outbreeding causes sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98:329–336

    Article  CAS  PubMed  Google Scholar 

  • Rasband WS (1997–2014) ImageJ, US National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997–2014

  • Reed DA, Luhring KA, Stafford CA, Hansen AK, Millar JG, Hanks LM, Paine TD (2007) Host defensive response against egg parasitoid involves cellular encapsulation response and melanization. Biol Contr 41:214–222

    Article  Google Scholar 

  • Rigaud T, Perrot-Minnot MJ, Brown MJF (2010) Parasite and host assemblages: embracing reality will improve our knowledge of transmission and virulence. Proc R Soc B Bio 277:3693–3702

    Article  Google Scholar 

  • Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301:472–475

    Article  CAS  PubMed  Google Scholar 

  • Ryder JJ (2007) Temporal dynamics of the encapsulation response towards a synthetic immune challenge in Acheta domesticus. Physiol Entomol 32:240–245

    Article  Google Scholar 

  • Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B Bio 270:357–366

    Article  Google Scholar 

  • Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P, Durrer S (1991) Parasites, floral resources, and reproduction in natural-populations of bumblebees. Oikos 62:342–350

    Article  Google Scholar 

  • Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

    Article  Google Scholar 

  • Schmid-Hempel R, Schmid-Hempel P (1996a) Host choice and fitness correlates for conopid flies parasitizing bumblebees. Oecologia 107:71–78

    Article  Google Scholar 

  • Schmid-Hempel R, Schmid-Hempel P (1996b) Larval development of two parasitic flies (Conopidae) in the common host Bombus pascuorum. Ecol Entomol 21:63–70

    Article  Google Scholar 

  • Schmid-Hempel R, Tognazzo M (2010) Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J Eukaryot Microbiol 5:337–345

    Article  Google Scholar 

  • Schmid-Hempel P, Muller C, Schmid-Hempel R, Shykoff JA (1990) Frequency and ecological correlates of parasitism by conopid flies (Conopidae, Diptera) in populations of bumblebees. Insectes Soc 37:14–30

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trees 11(8):317–321

    CAS  Google Scholar 

  • Shenefelt RD (1972) Braconidae 4. Microgasterinae, Apanteles. Hymenopt Cat (Nov ed.) 7:429–668

    Google Scholar 

  • Silva RJ, Cividanes FJ, Pedroso EC, Sala SRD (2011) Host quality of different aphid species for rearing Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). Neotrop Entomol 40(4):477–482

    CAS  PubMed  Google Scholar 

  • Smilanich AM, Dyer LA, Gentry GL (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90:1434–1440

    Article  PubMed  Google Scholar 

  • Stoehr AM, Kokko H (2006) Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav Ecol 17:751–756

    Article  Google Scholar 

  • Stoepler TM, Castillo JC, Lill JT, Eleftherianos I (2013) Hemocyte density increases with developmental stage in an immune challenged forest caterpillar. PLoS One 8:e70978. doi:10.1371/journal.pone.0070978

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14

    Article  CAS  Google Scholar 

  • Strand MR, Obrycki JJ (1996) Host specificity of insect parasitoids and predators. Bioscience 46:422–429

    Article  Google Scholar 

  • Strand MR, Pech LL (1995) Immunological basis for compatibility in parasitoid-host relationships. Annu Rev Entomol 40:31–56

    Article  CAS  PubMed  Google Scholar 

  • Straub CS, Ives AR, Gratton C (2011) Evidence for a trade-off between host range breadth and host-use efficiency in aphid parasitoids. Am Nat 177:389–395

    Article  PubMed  Google Scholar 

  • Traynor RE, Mayhew PJ (2005) Host range in solitary versus gregarious parasitoids: a laboratory experiment. Entomol Exp Appl 117:41–49

    Article  Google Scholar 

  • Vainio L, Hakkarainen H, Rantala MJ, Sorvari J (2004) Individual variation in immune function in the ant Formica exsecta; effects of the nest, body size and sex. Evol Ecol 18:75–84

    Article  Google Scholar 

  • van Alphen JJM, Janssen ARM (1982) Host selection by Asobara tabida Nees (Braconidae; Alysiinae) a larval parasitoid of fruit inhabiting Drosophila species. 2. Host species selection. Neth J Zool 32:194–214

    Article  Google Scholar 

  • van der Most P, de Jong B, Parmentier HK, Verhulst S (2011) Tradeoff between growth and immune function: a meta-analysis of selection experiments. Funct Ecol 25:74–80

    Article  Google Scholar 

  • Vogelweith F, Thiéry D, Moret Y, Moreau J (2013) Immunocompetence increases with larval body size in a phytophagous moth. Physiol Entomol 38:219–225

    Article  CAS  Google Scholar 

  • Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, Pletcher SD, Strand MR, Partridge L, Godfray HCJ (2005) Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6:R94

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We gratefully acknowledge funding and support from Sigma Xi’s Grant-in-Aid of Research Program, the University of Virginia’s Ingrassia Family Research Grant for Echols Scholars, and the National Science Foundation’s FSML Program (DBI1034846). S. E. D. was supported by the University of Virginia’s College Science Scholars Program and Blandy Experimental Farm. We thank Dr David E. Carr for his careful review of the statistical analyses in this paper. For their technical assistance in the field and laboratory we thank Amber Slatosky, Ariel Firebaugh, Courtney Beach, Megan Huff, and Kellen Paine. We also thank two anonymous referees whose comments improved this manuscript.

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The authors declare no conflict of interest in the execution or publication of this research.

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Correspondence to Rosemary L. Malfi.

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Communicated by George Heimpel.

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Davis, S.E., Malfi, R.L. & Roulston, T.H. Species differences in bumblebee immune response predict developmental success of a parasitoid fly. Oecologia 178, 1017–1032 (2015). https://doi.org/10.1007/s00442-015-3292-8

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