Animals; Aphids/microbiology; Aphids/physiology; Entomophthorales/pathogenicity; Female; Life Cycle Stages; Poaceae; Symbiosis; Aphids; Entomophthorales; Ecology, Evolution, Behavior and Systematics; Insect Science
Abstract :
[en] Pandora neoaphidis and Entomophthora planchoniana are widespread and important specialist fungal pathogens of aphids in cereals (Sitobion avenae and Rhopalosiphum padi). The two aphid species share these pathogens and we compare factors influencing susceptibility and resistance. Among factors that may influence susceptibility and resistance are aphid behavior, conspecific versus heterospecific host, aphid morph, life cycle, and presence of protective endosymbionts. It seems that the conspecific host is more susceptible (less resistant) than the heterospecific host, and alates are more susceptible than apterae. We conceptualize the findings in a diagram showing possible transmission in field situations and we pinpoint where there are knowledge gaps.
Precision for document type :
Review article
Disciplines :
Entomology & pest control
Author, co-author :
Eilenberg, Jørgen; Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark. Electronic address: jei@plen.ku.dk
Saussure, Stéphanie; Norwegian Institute of Bioeconomy Research (NIBIO), Division of Biotechnology and Plant Health, P.O. Box 115, NO-1431 Ås, Norway, Norwegian University of Life Sciences, Department of Plant Science, P.O. Box 5003, NO-1432 Ås, Norway
Ben Fekih, Ibtissem ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Jensen, Annette Bruun; Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
Klingen, Ingeborg; Norwegian Institute of Bioeconomy Research (NIBIO), Division of Biotechnology and Plant Health, P.O. Box 115, NO-1431 Ås, Norway
Language :
English
Title :
Factors driving susceptibility and resistance in aphids that share specialist fungal pathogens.
Stéphanie Saussure and Ingeborg Klingen were supported by the Research Council of Norway through the SMARTCROP project (project number 244526). We thank Mark Goettel for many useful comments to the manuscript.
Hajek, A.E., Shapiro-Ilan, D.I., General concepts in the ecology of invertebrate diseases. Hajek, A.E., Shapiro-Ilan, D.I., (eds.) Ecology of Invertebrate Diseases, 2018, Wiley, 3–18 The concepts of epidemiology of invertebrate diseases are outlined, including definitions of terms like pathogenicity and virulence when applied to invertebrate diseases.
Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E., Pell, J.K., Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Ann Rev Entomol 51 (2006), 331–357.
De Fine Licht, H.H., Does pathogens plasticity facilitate host shifts?. PLoS Pathog, 14, 2018, e1006961 The author highlights non-adaptive plasticity or genetic variation in the pathogen population.
Jensen, A.B., Eilenberg, J., Lastra, C.L., Differential divergences of obligately insect-pathogenic Entomophthora species from fly and aphid hosts. FEMS Microbiol Lett 300 (2009), 180–187.
Blackman, R.L., Eastop, V.F., Taxonomic issues. van Emden, H.F., Harrington, R., (eds.) Aphids as Crop Pests, 2007, CABI, Wallingford, United Kingdom, 18–20.
Dedryver, C.A., Legallic, J.F., Gauthier, J.P., Simon, J.C., Life cycle of the cereal aphid Sitobion avenae F.: polymorphism and comparison of life history traits associated with sexuality. Ecol Entomol 23 (1998), 123–132.
Halkett, F., Harrington, R., Hullé, M., Kindlmann, P., Menu, F., Rispe, C., Plantegenest, M., Dynamics of production of sexual forms in aphids: theoretical and experimental evidence for adaptive “coin‐flipping” plasticity. Am Nat 163 (2004), E112–E125, 10.1086/383618.
Rispe, C., Bonhomme, J., Simon, J.-C., Extreme life-cycle and sex ratio variation among sexually produced clones of the aphid Rhopalosiphum padi (Homoptera: Aphididae). Oikos 86 (1999), 254–264.
Klingauf, F.A., Feeding, adaptation and excretion. Minks, A.K., Harrewijn, P., (eds.) Aphids. Their Biology, Natural Enemies and Control, Vol A, 1987, Elsevier, 225–254.
Nielsen, G.C., Jensen, J.P., Crop Diseases and Pests (In Danish). 2005, Dansk Landbrugsskoles Forlag.
Haack, L., Simon, J.C., Gauthier, J.P., Plantegenest, M., Dedryver, C.A., Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Mol Ecol 9 (2000), 2055–2066.
Dedryver, C.A., Fiévet, V., Plantegenest, M., Vialatte, A., An overview of the functioning of Sitobion avenae populations at three spatial scales in France. Redia 92 (2009), 159–162.
Thaxter, R., The Entomophthoraceae of the United States. Memoirs Boston Soc Nat Hist 4 (1888), 134–201 plus 21 plates.
Butt, T.M., Beckett, A., Wilding, N., Protoplasts in the in vivo life cycle of Erynia neoaphidis. J Gen Microbiol 127 (1981), 417–421.
Eilenberg, J., Bresciani, J., Latgé, J.P., Ultrastructural studies of primary spore formation and discharge in the genus Entomophthora. J Invertebr Pathol 48 (1986), 318–324.
Brobyn, P.J., Wilding, N., Invasive and developmental processes of Entomophthora species infecting aphids. Trans Br Mycol Soc 69 (1977), 349–366.
Butt, T.M., Beckett, A.S., Wilding, N., A histological study of the invasive and developmental processes of the aphid pathogen Erynia neoaphidis (Zygomycotina: Entomophthorales) in the pea aphid Acyrtosiphon pisum. Can J Bot 68 (1990), 2153–2163.
Eilenberg, J., Bresciani, J., Olesen, U., Olson, L., Ultrastructural studies of secondary spore formation and discharge in the genus Entomophthora. J Invertebr Pathol 65 (1995), 179–185.
Scorsetti, A.C., Jensen, A.B., Lastra, C.L., Humber, R.A., First report of Pandora resting spore formation in vivo in aphid hosts. Fung Biol 116 (2012), 196–203.
Nielsen, C., Steenberg, T., Entomophthoralean fungi infecting the bird cherry-oat aphid, Rhopalosiphum padi, feeding on its winter host bird cherry, Prunus padus. J Invertebr Pathol 87 (2004), 70–73.
Nielsen, C., Hajek, A.E., Humber, R.H., Bresciani, J., Eilenberg, J., Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biol Contr 28 (2003), 92–100.
Hemmati, F., McCartney, H.A., Deadman, M.L., Airborne concentrations of conidia of Erynia neoaphidis above cereal fields. Mycol Res 105 (2001), 485–489.
Lu, H.-L., St Leger, R.J., Insect immunity to entomopathogenic fungi. Adv Gen 94 (2016), 251–285.
Lundgren, J.A., Jurat-Fuentes, J.L., Physiology and ecology of host defence against microbial invaders. Vega, F.E., Kaya, H.K., (eds.) Insect Pathology, edn 2, 2012, Elsevier, Amsterdam, 461–480.
Małagocka, J., Jensen, A.B., Eilenberg, J., Pandora formicae, a specialist ant pathogenic fungus: new insights into biology and taxonomy. J Invertebr Pathol 143 (2017), 108–114 This article presents basic biological and taxonomic information about a specialist fungus pathogen from the genus Pandora and its interaction with its ant host.
Trandem, N., Bhattarai, U.R., Westrum, K., Knudsen, G.K., Klingen, I., Fatal attraction: male spider mites prefer females killed by the mite-pathogenic fungus Neozygites floridana. J Invertebr Pathol 128 (2015), 6–13.
Nielsen, C., Agrawal, A.A., Hajek, A.E., Ants defend aphids against lethal disease. Biol Lett 67 (2010), 205–208.
Grell, M.N., Jensen, A.B., Olsen, P.B., Eilenberg, J., Lange, L., Secretome of fungus-infected aphids documents high pathogen activity and weak host response. Fung Gen Biol 48 (2011), 343–352.
Saussure, S., Westrum, K., Hjelkrem, A.-G.R., Klingen, I., Effect of three isolates of Pandora neoaphidis from a single population of Sitobion avenae on mortality, speed of kill and fecundity of S. avenae and Rhopalosiphum padi at different temperatures. Fung Ecol 41 (2019), 1–12 This study yields information useful to model the population dynamics of P. neoaphidis and its hosts and increase our understanding of its epizootics and potential use in integrated pest management.
Hatano, E., Baverstock, J., Kunert, G., Pell, J.K., Weisser, W.W., Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids, Acyrthosiphon pisum (Hemiptera: Aphididae). Ecol Entomol 37 (2012), 75–82.
Parker, B.J., Barribeau, S.M., Laughton, A.M., Griffin, L.H., Gerardo, N.M., Life-history strategy determines constraints on immune function. J Anim Ecol 86 (2017), 473–483 Immune costs were limited to winged aphids. The authors suggest that such costs can reflect stronger investment in immunity since alates are at higher disease risk.
Dromph, K.M., Pell, J.K., Eilenberg, J., Influence of clone and morph on susceptibility of Sitobion avenae to infection by Erynia neoaphidis. Biocont Sci Technol 12 (2002), 753–756.
Jensen, A.B., Hansen, L.M., Eilenberg, J., Grain aphid population structure: no effect of fungal infections in a 2-year field study in Denmark. Agric For Entomol 10 (2008), 279–290.
Fakhour, S., Ambroise, J., Renoz, F., Foray, V., Gala, J.-L., Hance, T., A large-scale field study of bacterial communities in cereal aphid populations across Morocco. FEMS Microbiol Ecol, 94, 2018, 10.1093/femsec/fiy003.
Zepeda-Paulo, F., Ortiz-Martínez, S., Silva, A.X., Lavandero, B., Low bacterial community diversity in two introduced aphid pests revealed with 16S rRNA amplicon sequencing. PeerJ, 6, 2018, e4725, 10.7717/peerj.4725 A study showing natural occurrence of similar endosymbiotic bacteria in Sitobion avenae and Rhopalosiphum padi. The authors suggest that aphid-endosymbic associations can vary across the geographic range of an aphid species.
Douglas, A.E., Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Ann Rev Entomol 43 (1998), 17–37.
Łukasik, P., Dawid, M.A., Ferrari, J., Godfray, H.C.J., The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia, 173, 2013, 985996, 10.1007/s00442-013-2660-5.
Henry, L.M., Maiden, M.C., Ferrari, J., Godfray, H.C., Insect life history and the evolution of bacterial mutualism. Ecol Lett, 18, 2013, 516525, 10.1111/ele.12425.
Alkhedir, H., Karlovsky, P., Mashaly, A.M.A., Vidal, S., Phylogenetic relationships of the symbiotic bacteria in the aphid Sitobion avenae (Hemiptera: Aphididae). Environ Entomol, 44, 2015, 13581366, 10.1093/ee/nvv114.
Łukasik, P., Guo, H., van Asch, M., Ferrari, J., Godfray, H.C., Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J Evol Biol 26 (2013), 2654–2661.
Heyworth, E.R., Ferrari, J., A facultative endosymbiont in aphids can provide diverse ecological benefits. J Evol Biol 28 (2016), 1753–1760.
Hrček, J., Parker, B.J., McLean, A.H.C., Simon, J.-C., Mann, C.M., Godfray, C.J., Hosts do not simply outsource pathogen resistance to protective symbionts. Evolution 72 (2018), 1488–1499 The authors found that biotypes of A. pisum that more frequently carry protective symbionts have higher, rather than lower, levels of intrinsic resistance to P. neoaphidis. Further, within a biotype, there was no difference in intrinsic resistance between those clones that did and those that did not harbor a symbiont.
Hajek, A.E., Papierok, B., Eilenberg, J., Methods for study of the Entomophthorales. Lacey, L., (eds.) Manual of Techniques in Invertebrate Pathology, edn 2, 2012, Academic Press, 285–316.
Shah, P.A., Clark, S.J., Pell, J.K., Direct and indirect estimates of Pandora neoaphidis conidia in laboratory assays with aphids. J Invertebr Pathol 84 (2003), 145–147.
Ben Fekih, I., Jensen, A.B., Boukhris-Bouhachem, S., Pozsgai, G., Rezgui, S., Rensing, C., Eilenberg, J., Virulence of two entomophthoralean fungi, Pandora neoaphidis and Entomophthora planchoniana, to their conspecific (Sitobion avenae) and heterospecific (Rhopalosiphum padi) aphid hosts. Insects, 10, 2019, 10.3390/insects10020054.
Barta, M., Cagáň, L., Observations on the occurrence of Entomophthorales infecting aphids (Aphidoidea) in Slovakia. BioControl 51 (2006), 795–808.
Ben Fekih, I., Boukhris-Bouhachem, S., Eilenberg, J., Bechir Allagui, M., Jensen, A.B., The occurrence of two species of Entomophthorales (Entomophthoromycota), pathogens of Sitobion avenae and Myzus persicae (Hemiptera: Aphididae) in Tunisia. BioMed Res Int, 2013, 838145.
Ben Fekih, I., Boukhris-Bouhachem, S., Bechir Allagui, M., Jensen, A.B., Eilenberg, J., First survey on ecological host range of aphid pathogenic fungi (Phylum Entomophthoromycota) in Tunisia. Ann Soc Entomol Fr (N.S.) 51 (2015), 140–144.
Hatting, J.L., Poprawski, T.J., Miller, R.M., Prevalences of fungal pathogens and other natural enemies of cereal aphids (Homoptera: Aphididae) in wheat under dryland and irrigated conditions in South Africa. BioControl 45 (2000), 179–199.
Li, W., Sheng, C.-F., Occurrence and distribution of entomophthoralean fungi infecting aphids in mainland China. Biocont Sci Technol 17 (2007), 433–439.
Nielsen, C., Eilenberg, J., Harding, S., Oddsdottir, E., Haldorsson, G., Geographical distribution and host range of Entomophthorales infecting the green spruce aphid Elatobium abietinum Walker in Iceland. J Invertebr Pathol 78 (2001), 72–80.
Steenberg, T., Eilenberg, J., Natural occurrence of entomopathogenic fungi on aphids at an agricultural field site. Czech Mycol 48 (1995), 89–96.
Powell, W., Dean, G.J., Wilding, N., The influence of weeds on aphid-specific natural enemies in winter wheat. Crop Prot 5 (1986), 182–189.
Feng, M.-G., Chen, C., Chen, B., Wide dispersal of aphid-pathogenic Entomophthorales among aphids relies upon migratory alates. Environ Microbiol 6 (2004), 510–516.
Shah, P.A., Clark, S.J., Pell, J.K., Assessment of aphid host range and isolate variability in Pandora neoaphidis (Zygomycetes: Entomophthorales). Biol Cont 29 (2004), 90–99.
Sletteng, C., Aphids and their Natural Enemies (Hymenoptera and Entomophthorales) in Cereals - Population Dynamics, Prevalence and Effect of Insect Pathogenic Fungi. MSc Thesis. 2014, Norwegian University of Life Sciences.
Nielsen, C., Eilenberg, J., Dromph, K.M., Entomophthorales on Cereal Aphids: Characterisation, Growth, Virulence, Epizootiology and Potential for Microbial Control. 2001, Danish Environmental Protection Agency, The Ministry of Environment and Energy, Copenhagen, Denmark Pesticides Research No. 53, 76 pp.