Aphid-encoded variability in susceptibility to a parasitoid

BMC Evolutionary Biology

Kerry M Oliver²  Jacob A Russell¹  Matthew R Doremus²  Shannon G Ritter²  Adam J Martinez² 

[1]Department of Biology, Drexel University, Philadelphia PA 19104, USA

[2]Department of Entomology, University of Georgia, Athens GA 30602, USA

关键词: Immunity;    Fecundity;    Selection;    Symbiont;    Trade-off;    Resistance;   

Others  :  855329
DOI  :  10.1186/1471-2148-14-127

 received in 2014-03-28, accepted in 2014-05-27,  发布年份 2014

【 摘 要 】

Background

Many animals exhibit variation in resistance to specific natural enemies. Such variation may be encoded in their genomes or derived from infection with protective symbionts. The pea aphid, Acyrthosiphon pisum, for example, exhibits tremendous variation in susceptibility to a common natural enemy, the parasitic wasp Aphidius ervi. Pea aphids are often infected with the heritable bacterial symbiont, Hamiltonella defensa, which confers partial to complete resistance against this parasitoid depending on bacterial strain and associated bacteriophages. That previous studies found that pea aphids without H. defensa (or other symbionts) were generally susceptible to parasitism, together with observations of a limited encapsulation response, suggested that pea aphids largely rely on infection with H. defensa for protection against parasitoids. However, the limited number of uninfected clones previously examined, and our recent report of two symbiont-free resistant clones, led us to explicitly examine aphid-encoded variability in resistance to parasitoids.

Results

After rigorous screening for known and unknown symbionts, and microsatellite genotyping to confirm clonal identity, we conducted parasitism assays using fifteen clonal pea aphid lines. We recovered significant variability in aphid-encoded resistance, with variation levels comparable to that contributed by H. defensa. Because resistance can be costly, we also measured aphid longevity and cumulative fecundity of the most and least resistant aphid lines under permissive conditions, but found no trade-offs between higher resistance and these fitness parameters.

Conclusions

These results indicate that pea aphid resistance to A. ervi is more complex than previously appreciated, and that aphids employ multiple tactics to aid in their defense. While we did not detect a tradeoff, these may become apparent under stressful conditions or when resistant and susceptible aphids are in direct competition. Understanding sources and amounts of variation in resistance to natural enemies is necessary to understand the ecological and evolutionary dynamics of antagonistic interactions, such as the potential for coevolution, but also for the successful management of pest populations through biological control.

【 授权许可】

   
2014 Martinez et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Fellowes MDE, Kraaijeveld AR, Godfray HCJ: Association between feeding rate and parasitoid resistance in Drosophila melanogaster. Evolution 1999, 53(4):1302-1305.
• [2]Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ: Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 2010, 329(5988):212-215.
• [3]Oliver KM, Campos J, Moran NA, Hunter MS: Population dynamics of defensive symbionts in aphids. Proc Biol Sci 2008, 275(1632):293-299.
• [4]Moller AP: Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 1990, 44(4):771-784.
• [5]Spitze K: Predator-mediated plasticity of prey life history and morphology: Chaoborus americanus predation on Daphnia pulex. Am Nat 1992, 139(2):229-247.
• [6]Grosholz ED: The effects of host genotype and spatial distribution on trematode parasitism in a bivalve population. Evolution 1994, 48(5):1514-1524.
• [7]Boulinier T, Sorci G, Monnat JY, Danchin E: Parent‒offspring regression suggests heritable susceptibility to ectoparasites in a natural population of kittiwake Rissa tridactyla. J Evol Biol 1997, 10(1):77-85.
• [8]Ebert D, Zschokke-Rohringer CD, Carius HJ: Within–and between–population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proc R Soc Lond B Biol Sci 1998, 265(1410):2127-2134.
• [9]Brinkhof MW, Heeb P, Kölliker M, Richner H: Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc R Soc Lond B Biol Sci 1999, 266(1435):2315-2322.
• [10]Smith JA, Wilson K, Pilkington JG, Pemberton JM: Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proc R Soc Lond B Biol Sci 1999, 266(1425):1283-1290.
• [11]Carius HJ, Little TJ, Ebert D: Genetic variation in a host‒parasite association: potential for coevolution and frequency‒dependent selection. Evolution 2001, 55(6):1136-1145.
• [12]Martinez AJ, Weldon SR, Oliver KM: Effects of parasitism on aphid nutritional and protective symbioses. Mol Ecol 2014, 23(6):1594-1607.
• [13]Sadd BM, Schmid-Hempel P: Principles of ecological immunology. Evol Appl 2009, 2(1):113-121.
• [14]Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM: Non-immunological defense in an evolutionary framework. Trends Ecol Evol 2011, 26(5):242-248.
• [15]Evison SEF, Fazio G, Chappell P, Foley K, Jensen AB, Hughes WOH: Host-parasite genotypic interactions in the honey bee: the dynamics of diversity. Ecol Evol 2013, 3(7):2214-2222.
• [16]Sadd BM, Barribeau SM: Heterogeneity in infection outcome: lessons from a bumblebee-trypanosome system. Parasite Immunol 2013, 35(11):339-349.
• [17]Rolff J, Siva-Jothy MT: Invertebrate ecological immunology. Science 2003, 301(5632):472-475.
• [18]Schmid-Hempel P: Evolutionary ecology of insect immune defenses. Annu Rev Entomol 2005, 50:529-551.
• [19]Sutter GR, Rothenbuhler WC, Raun ES: Resistance to American foulbrood in honey bees: VII. Growth of resistant and susceptible larvae. J Invertebr Pathol 1968, 12(1):25-28.
• [20]Yan G, Severson DW, Christensen BM: Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 1997, 51(2):441-450.
• [21]Kraaijeveld A, Godfray H: Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 1997, 389(6648):278-280.
• [22]Boots M, Begon M: Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct Ecol 1993, 7(5):528-534.
• [23]Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT: Examining costs of induced and constitutive immune investment in Tenebrio molitor. J Evol Biol 2003, 16(5):1038-1044.
• [24]Webster J, Woolhouse M: Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system. Proc R Soc Lond B Biol Sci 1999, 266(1417):391-396.
• [25]Chaboudez P, Burdon J: Frequency-dependent selection in a wild plant-pathogen system. Oecologia 1995, 102(4):490-493.
• [26]Koskella B, Lively CM: Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and sterilizing trematode. Evolution 2009, 63(9):2213-2221.
• [27]Foster SP, Tomiczek M, Thompson R, Denholm I, Poppy G, Kraaijeveld AR, Powell W: Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack. Anim Behav 2007, 74(3):621-632.
• [28]Bryan-Walker K, Leung TL, Poulin R: Local adaptation of immunity against a trematode parasite in marine amphipod populations. Mar Biol 2007, 152(3):687-695.
• [29]Sanders AE, Scarborough C, Layen SJ, Kraaijeveld AR, Godfray HCJ: Evolutionary change in parasitoid resistance under crowded conditions in Drosophila melanogaster. Evolution 2005, 59(6):1292-1299.
• [30]Luong L, Polak M: Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system. Heredity 2007, 99(6):632-640.
• [31]Triggs A, Knell RJ: Interactions between environmental variables determine immunity in the Indian meal moth Plodia interpunctella. J Anim Ecol 2012, 81(2):386-394.
• [32]Godfray HCJ: Parasitoids: Behavioral and Evolutionary Ecology. Princeton: Princeton University Press; 1994.
• [33]Kraaijeveld AR, Godfray HCJ: Evolution of Host Resistance and Parasitoid Counter-Resistance. In Advances in Parasitology, Vol 70: Parasitoids of Drosophila, Volume 70 Edited by Prevost G. 2009, 257-280.
• [34]Le Ralec A, Anselme C, Outreman Y, Poirie M, van Baaren J, Le Lann C, van Alphen JJM: Evolutionary ecology of the interactions between aphids and their parasitoids. C R Biol 2010, 333(6–7):554-565.
• [35]Henter HJ, Via S: The potential for coevolution in a host-parasitoid system 1. Genetic variation within a an aphid population in susceptibility to a parasitic wasp. Evolution 1995, 49(3):427-438.
• [36]Ferrari J, Muller CB, Kraaijeveld AR, Godfray HCJ: Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 2001, 55(9):1805-1814.
• [37]Gwynn DM, Callaghan A, Gorham J, Walters KFA, Fellowes MDE: Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proc R Soc Lond B Biol Sci 2005, 272(1574):1803-1808.
• [38]Stacey DA, Fellowes MDE: Influence of temperature on pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) resistance to natural enemy attack. Bull Entomol Res 2002, 92(4):351-357.
• [39]Oliver KM, Russell JA, Moran NA, Hunter MS: Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 2003, 100(4):1803-1807.
• [40]Bensadia F, Boudreault S, Guay JF, Michaud D, Cloutier C: Aphid clonal resistance to a parasitoid fails under heat stress. J Insect Physiol 2006, 52(2):146-157.
• [41]Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE: Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 2004, 29(1):60-65.
• [42]Guay JF, Boudreault S, Michaud D, Cloutier C: Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J Insect Physiol 2009, 55(10):919-926.
• [43]Oliver KM, Degnan PH, Hunter MS, Moran NA: Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009, 325(5943):992-994.
• [44]Oliver KM, Moran NA, Hunter MS: Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci 2005, 102(36):12795-12800.
• [45]Oliver KM, Moran NA, Hunter MS: Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc Lond B Biol Sci 2006, 273(1591):1273-1280.
• [46]Degnan PH, Moran NA: Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 2008, 74(21):6782-6791.
• [47]Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H: The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci U S A 2005, 102(47):16919-16926.
• [48]Carver M, Sullivan DJ: Encapsulative Defense Reactions of Aphids (Hemiptera: Aphididae) to Insect Parasitoids (Hymenoptera: Aphidiidae and Aphelinidae) (Minireview). In Ecology and Effectiveness of Aphidophaga. Edited by Niemczyk E, Dixon AFG. The Netherlands: SPB Academic; 1988:299-303.
• [49]Laughton AM, Garcia JR, Altincicek B, Strand MR, Gerardo NM: Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. J Insect Physiol 2011, 57(6):830-839.
• [50]Vorburger C, Gehrer L, Rodriguez P: A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 2010, 6(1):109-111.
• [51]von Burg S, Ferrari J, Müller CB, Vorburger C: Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs. Proc R Soc Lond B Biol Sci 2008, 275(1638):1089-1094.
• [52]Sandrock C, Gouskov A, Vorburger C: Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host-parasitoid interaction. J Evol Biol 2010, 23(3):578-585.
• [53]Caillaud MC, Via S: Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am Nat 2000, 156(6):606-621.
• [54]Ferrari J, Godfray HCJ, Faulconbridge AS, Prior K, Via S: Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution 2006, 60(8):1574-1584.
• [55]Ferrari J, Scarborough CL, Godfray HCJ: Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 2007, 153(2):323-329.
• [56]Ferrari J, Via S, Godfray HCJ: Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 2008, 62(10):2508-2524.
• [57]Frantz A, Plantegenest M, Mieuzet L, Simon JC: Ecological specialization correlates with genotypic differentiation in sympatric host-populations of the pea aphid. J Evol Biol 2006, 19(2):392-401.
• [58]Peccoud J, Simon JC, McLaughlin HJ, Moran NA: Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proc Natl Acad Sci U S A 2009, 106(38):16315-16320.
• [59]Hufbauer RA, Via S: Evolution of an aphid-parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 1999, 53(5):1435-1445.
• [60]Via S, Bouck AC, Skillman S: Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 2000, 54(5):1626-1637.
• [61]Eastop VF: A taxonomic study of australian aphidoidea (Homoptera). Aust J Zool 1966, 14(3):399-592.
• [62]Brisson JA, Nuzhdin SV, Stern DL: Similar patterns of linkage disequilibrium and nucleotide diversity in native and introduced populations of the pea aphid, Acyrthosiphon pisum. BMC Genet 2009, 10:22.
• [63]Ferrari J, West JA, Via S, Godfray HCJ: Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 2012, 66(2):375-390.
• [64]Russell JA, Weldon S, Smith AH, Kim KL, Hu Y, Łukasik P, Doll S, Anastopoulos I, Novin M, Oliver KM: Uncovering symbiont‒driven genetic diversity across North American pea aphids. Mol Ecol 2013, 22(7):2045-2059.
• [65]Lamb R, Pointing P: Sexual morph determination in the aphid, Acyrthosiphon pisum. J Insect Physiol 1972, 18(10):2029-2042.
• [66]Sandstrom JP, Russell JA, White JP, Moran NA: Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology 2001, 10(1):217-228.
• [67]Richards S, Gibbs RA, Gerardo NM, Moran N, Nakabachi A, Stern D, Tagu D, Wilson ACC, Muzny D, Kovar C, et al.: Genome sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol 2010, 8(2):24.
• [68]Parker BJ, Garcia JR, Gerardo NM: Genetic variation in resistance and fecundity tolerance in a natural host–pathogen interaction. Evolution 2014. in press
• [69]Barribeau SM, Sok D, Gerardo NM: Aphid reproductive investment in response to mortality risks. BMC Evol Biol 2010, 10:11. BioMed Central Full Text
• [70]Angalet G, Fuester R: The Aphidius parasites of the pea aphid Acyrthosiphon pisum in the eastern half of the United States. Ann Entomol Soc Am 1977, 70(1):87-96.
• [71]Kurokawa T, Yao I, Akimoto S, Hasegawa E: Isolation of six microsatellite markers from the pea aphid, Acyrthosiphon pisum (Homoptera, Aphididae). Mol Ecol Notes 2004, 4(3):523-524.
• [72]Caillaud M, Mondor‒Genson G, Levine‒Wilkinson S, Mieuzet L, Frantz A, Simon J, D’Acier Coeur A: Microsatellite DNA markers for the pea aphid Acyrthosiphon pisum. Mol Ecol Notes 2004, 4(3):446-448.
• [73]Henter HJ: The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid host. Evolution 1995, 49(3):439-445.
• [74]Dion E, Zele F, Simon JC, Outreman Y: Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J Evol Biol 2011, 24(4):741-750.
• [75]Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX, Hunter MS: Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol 2012, 10(1):11. BioMed Central Full Text
• [76]Nyabuga FN, Outreman Y, Simon JC, Heckel DG, Weisser WW: Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomol Exp Appl 2010, 136(3):243-253.
• [77]Bilodeau E, Simon JC, Guay JF, Turgeon J, Cloutier C: Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi? Evol Ecol 2013, 27(1):165-184.
• [78]Oliver KM, Smith AH, Russell JA: Defensive symbiosis in the real world – advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 2014, 28(2):341-355.
• [79]Strand MR, Pech LL: Immunological basis for compatibility in parasitoid host relationships. Annu Rev Entomol 1995, 40:31-56.
• [80]Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, De Vos M, Duncan EJ, Evans JD, Gabaldon T, Ghanim M, Heddi A, Kaloshian I, Latorre A, Moya A, Nakabachi A, Parker BJ, Perez-Brocal V, Pignatelli M, Rahbe Y, Ramsey JS, Spragg CJ, Tamames J, Tamarit D, Tamborindeguy C, Vincent-Monegat C, Vilcinskas A: Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 2010, 11(2):R21. BioMed Central Full Text
• [81]Lukasik P, van Asch M, Guo HF, Ferrari J, Godfray HCJ: Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 2013, 16(2):214-218.
• [82]Parker BJ, Spragg CJ, Altincicek B, Gerardo NM: Symbiont-mediated protection against fungal pathogens in Pea Aphids: a role for pathogen specificity? Appl Environ Microbiol 2013, 79(7):2455-2458.
• [83]Scarborough CL, Ferrari J, Godfray HCJ: Aphid protected from pathogen by endosymbiont. Science 2005, 310(5755):1781-1781.
• [84]Schmid M, Sieber R, Zimmermann YS, Vorburger C: Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct Ecol 2012, 26(1):207-215.
• [85]Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE: Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 2009, 160(2):387-398.
• [86]Cayetano L, Vorburger C: Genotype-by-genotype specificity remains robust to average temperature variation in an aphid/endosymbiont/parasitoid system. J Evol Biol 2013, 26(7):1603-1610.
• [87]Rouchet R, Vorburger C: Strong specificity in the interaction between parasitoids and symbiont-protected hosts. J Evol Biol 2012, 25(11):2369-2375.
• [88]Moran NA: The evolution of aphid life-cycles. Annu Rev Entomol 1992, 37:321-348.
• [89]Martinez AJ, Ritter SG, Doremus MR, Russell JA, Oliver KM: Data from: Aphid-encoded variability in susceptibility to a parasitoid. Dryad Data Repository 2014. http://dx.doi.org/10.5061/dryad.6b5f0 webcite