Section: Ecology
Topic: Ecology, Biology of interactions

Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps

10.24072/pcjournal.8 - Peer Community Journal, Volume 1 (2021), article no. e12.

Get full text PDF Peer reviewed and recommended by PCI

When organisms coevolve, any change in one species can affect phenotypes and ecology of the other species. Upper trophic levels have to synchronize their life-cycle to both abiotic conditions and lower trophic level species phenotypic variations and phenology. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. We tested the effect of seasonal variation in host quality on parasitoid diapause induction by using viviparous and oviparous female morphs of the pea aphid Acyrthosiphon pisum. Aphidius ervi parasitoids from two populations of contrasted climatic origin (harsh vs. mild winter areas) were allowed to parasitize each morph in a split-brood design and were next reared under either fall-like or summer-like temperature-photoperiod conditions. We found that oviparous morphs, present before winter, are cues per se for diapause induction; parasitoids entered diapause at higher levels when developing in oviparous hosts (19.4 3.0%) than in viviparous ones (3.6 1.3%), under summer-like conditions (i.e., when oviparous aphids appear in the fields). This pattern was only observed in parasitoids from the harsh winter area, suggesting local adaptations to variation in host quality as an overwintering cue. Analyses of the relative proportion of forty-seven metabolites and lipid reserves in both aphid morphs produced under the same conditions suggest parasitoids response to be mainly influenced by chemical cues derived from the host, with higher proportion of polyols and sugars, and more fat reserves being found in oviparous morphs. Host physiological state thus varies across the seasons and represents one of the multiple environmental indicators of upcoming detrimental conditions, affecting parasitoid overwintering strategies and diapause. Our results underline coevolutionary processes between hosts and parasitoids in their area of origin, likely leading to phenological synchronization with the environment. We point out the importance of such bottom-up effects for ecosystem functioning and for the provision of ecosystem services such as biological control.

Published online:
DOI: 10.24072/pcjournal.8
Type: Research article
Tougeron, Kévin 1, 2; Brodeur, Jacques 1; van Baaren, Joan 2; Renault, David 3, 2; Le Lann, Cécile 2

1 Institut de Recherche en Biologie Végétale, Département de Sciences Biologiques, Université de Montréal, 4101 rue Sherbrooke Est, Montréal, QC, Canada, H1X 2B2.
2 Univ Rennes, CNRS, ECOBIO (Ecosystèmes, biodiversité, évolution) - UMR 6553, 263 Avenue du Général Leclerc, F-35000 Rennes, France.
3 Institut Universitaire de France, 1 rue Descartes, 75231 Paris Cedex 05, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Tougeron, K\'evin and Brodeur, Jacques and van Baaren, Joan and Renault, David and Le Lann, C\'ecile},
     title = {Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps},
     journal = {Peer Community Journal},
     eid = {e12},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.8},
     url = {}
AU  - Tougeron, Kévin
AU  - Brodeur, Jacques
AU  - van Baaren, Joan
AU  - Renault, David
AU  - Le Lann, Cécile
TI  - Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.8
ID  - 10_24072_pcjournal_8
ER  - 
%0 Journal Article
%A Tougeron, Kévin
%A Brodeur, Jacques
%A van Baaren, Joan
%A Renault, David
%A Le Lann, Cécile
%T Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.8
%F 10_24072_pcjournal_8
Tougeron, Kévin; Brodeur, Jacques; van Baaren, Joan; Renault, David; Le Lann, Cécile. Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps. Peer Community Journal, Volume 1 (2021), article  no. e12. doi : 10.24072/pcjournal.8.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100022

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agrawal, A. A. Phenotypic Plasticity in the Interactions and Evolution of Species, Science, Volume 294 (2001) no. 5541, pp. 321-326 | DOI

[2] Andrade, T. O.; Krespi, L.; Bonnardot, V.; van Baaren, J.; Outreman, Y. Impact of change in winter strategy of one parasitoid species on the diversity and function of a guild of parasitoids, Oecologia, Volume 180 (2015) no. 3, pp. 877-888 | DOI

[3] Andrade, T. O.; Outreman, Y.; Krespi, L.; Plantegenest, M.; Vialatte, A.; Gauffre, B.; van Baaren, J. Spatiotemporal variations in aphid-parasitoid relative abundance patterns and food webs in agricultural ecosystems, Ecosphere, Volume 6 (2015) no. 7 | DOI

[4] Archetti, M.; Döring, T. F.; Hagen, S. B.; Hughes, N. M.; Leather, S. R.; Lee, D. W.; Lev-Yadun, S.; Manetas, Y.; Ougham, H. J.; Schaberg, P. G.; Thomas, H. Unravelling the evolution of autumn colours: an interdisciplinary approach, Trends in Ecology & Evolution, Volume 24 (2009) no. 3, pp. 166-173 | DOI

[5] Arrese, E. L.; Soulages, J. L. Insect Fat Body: Energy, Metabolism, and Regulation, Annual Review of Entomology, Volume 55 (2010) no. 1, pp. 207-225 | DOI

[6] van Baaren, J.; Nénon, J.-P. Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae, Entomologia Experimentalis et Applicata, Volume 81 (1996) no. 1, pp. 61-69 | DOI

[7] Bale, J. S. Insects and low temperatures: from molecular biology to distributions and abundance, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Volume 357 (2002) no. 1423, pp. 849-862 | DOI

[8] Bale, J. S.; Hayward, S. A. L. Insect overwintering in a changing climate, Journal of Experimental Biology, Volume 213 (2010) no. 6, pp. 980-994 | DOI

[9] Boivin, G.; Hance, T.; Brodeur, J. Aphid parasitoids in biological control, Canadian Journal of Plant Science, Volume 92 (2012) no. 1, pp. 1-12 | DOI

[10] Bradshaw, W. E.; Holzapfel, C. M. Genetic shift in photoperiodic response correlated with global warming, Proceedings of the National Academy of Sciences, Volume 98 (2001) no. 25, pp. 14509-14511 | DOI

[11] Brodeur, J.; McNeil, J. N. Biotic and abiotic factors involved in diapause induction of the parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae), Journal of Insect Physiology, Volume 35 (1989) no. 12, pp. 969-974 | DOI

[12] Brodeur, J.; Mcneil, J. N. Seasonal Ecology of Aphidius nigripes (Hymenoptera: Aphidiidae), a Parasitoid of Macrosiphum euphorbiae (Homoptera: Aphididae), Environmental Entomology, Volume 23 (1994) no. 2, pp. 292-298 | DOI

[13] Brough, C.; Dixon, A. Ultrastructural features of egg development in oviparae of the vetch aphid, Megoura viciae buckton, Tissue and Cell, Volume 22 (1990) no. 1, pp. 51-63 | DOI

[14] Chippendale, G. M. Hormonal Regulation of Larval Diapause, Annual Review of Entomology, Volume 22 (1977) no. 1, pp. 121-138 | DOI

[15] Christiansen-Weniger, P.; Hardie, J. Development of the aphid parasitoid,Aphidius ervi, in asexual and sexual females of the pea aphid,Acyrthosiphon pisum, and the blackberry-cereal aphid,Sitobion fragariae, Entomophaga, Volume 42 (1997) no. 1-2, pp. 165-172 | DOI

[16] Christiansen-Weniger, P.; Hardie, J. Environmental and physiological factors for diapause induction and termination in the aphid parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae), Journal of Insect Physiology, Volume 45 (1999) no. 4, pp. 357-364 | DOI

[17] COLINET, H.; MURATORI, F.; HANCE, T. Cold-induced expression of diapause in Praon volucre: fitness cost and morpho-physiological characterization, Physiological Entomology, Volume 35 (2010) no. 4, pp. 301-307 | DOI

[18] Colinet, H.; Renault, D.; Charoy-Guével, B.; Com, E. Metabolic and Proteomic Profiling of Diapause in the Aphid Parasitoid Praon volucre, PLoS ONE, Volume 7 (2012) no. 2 | DOI

[19] Colinet, H.; Vernon, P.; Hance, T. Does thermal-related plasticity in size and fat reserves influence supercooling abilities and cold-tolerance in Aphidius colemani (Hymenoptera: Aphidiinae) mummies?, Journal of Thermal Biology, Volume 32 (2007) no. 7-8, pp. 374-382 | DOI

[20] Danks, H. V. Insect Dormancy: An Ecological Perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa, ON, Canada., 1987

[21] Dedryver, C.-A.; Hullé, M.; Le Gallic, J.-F.; Caillaud, M. C.; Simon, J.-C. Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae, Oecologia, Volume 128 (2001) no. 3, pp. 379-388 | DOI

[22] Denlinger, D. L. Regulation of Diapause, Annual Review of Entomology, Volume 47 (2002) no. 1, pp. 93-122 | DOI

[23] Dillwith, J. W.; Neese, P. A.; Brigham, D. L. Lipid biochemistry in aphids In: Insect Lipids: chemistry, biochemistry, and biology. Stanley D.W. & Nelson D.R. (eds.). (1993), pp. 389-434

[24] Dixon, A. F. G. Aphid Ecology An optimization approach, Springer Netherlands, Dordrecht, 1985 | DOI

[25] Ellers, J.; Toby Kiers, E.; Currie, C. R.; McDonald, B. R.; Visser, B. Ecological interactions drive evolutionary loss of traits, Ecology Letters, Volume 15 (2012) no. 10, pp. 1071-1082 | DOI

[26] Ellers, J.; Van Alphen, J. J. M. A trade-off between diapause duration and fitness in female parasitoids, Ecological Entomology, Volume 27 (2002) no. 3, pp. 279-284 | DOI

[27] Fordyce, J. A. The evolutionary consequences of ecological interactions mediated through phenotypic plasticity, Journal of Experimental Biology, Volume 209 (2006) no. 12, pp. 2377-2383 | DOI

[28] Gariepy, V.; Boivin, G.; Brodeur, J. Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions, Biological Control, Volume 80 (2015), pp. 1-7 | DOI

[29] Gerling, D.; Erel, E.; Guershon, M.; Inbar, M. Bionomics of Encarsia scapeata Rivnay (Hymenoptera: Aphelinidae), tritrophic relationships and host-induced diapause, Biological Control, Volume 49 (2009) no. 3, pp. 201-206 | DOI

[30] Godfray, H. C. J. Parasitoids, Princeton University Press, Princeton, NJ, 1994 | DOI

[31] Greenway, A.; Griffiths, D.; Furk, C.; Prior, R. Composition of triglycerides from aphids of six different families and from different seasonal forms of Aphis evonymi, Journal of Insect Physiology, Volume 20 (1974) no. 12, pp. 2423-2431 | DOI

[32] Hahn, D. A.; Denlinger, D. L. Energetics of Insect Diapause, Annual Review of Entomology, Volume 56 (2011) no. 1, pp. 103-121 | DOI

[33] Hardie, J. Juvenile hormone mimics the photoperiodic apterization of the alate gynopara of aphid, Aphis fabae, Nature, Volume 286 (1980) no. 5773, pp. 602-604 | DOI

[34] Hayward, S.; Pavlides, S.; Tammariello, S.; Rinehart, J.; Denlinger, D. Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence, Journal of Insect Physiology, Volume 51 (2005) no. 6, pp. 631-640 | DOI

[35] HODKOVA, M.; HODEK, I. Photoperiod, diapause and cold-hardiness, European Journal of Entomology, Volume 101 (2004) no. 3, pp. 445-458 | DOI

[36] Höller, C. Overwintering and hymenopterous parasitism in autumn of the cereal aphidSitobion avenae(F.) in northern FR Germany, Journal of Applied Entomology, Volume 109 (1990) no. 1-5, pp. 21-28 | DOI

[37] Hufbauer, R. A.; Bogdanowicz, S. M.; Harrison, R. G. The population genetics of a biological control introduction: mitochondrial DNA and microsatellie variation in native and introduced populations ofAphidus ervi, a parisitoid wasp, Molecular Ecology, Volume 13 (2004) no. 2, pp. 337-348 | DOI

[38] Hughes, L. Climate Change Impacts on Species Interactions: Assessing the Threat of Cascading Extinctions, Saving a Million Species, Island Press/Center for Resource Economics, Washington, DC, 2012, pp. 337-359 | DOI

[39] Hullé, M.; Turpeau, E.; Chaubet, B. Encyclop’aphid, a key for aphids and their parasitoids. INRA, 2006


[41] Iperti, G.; Hodek, I. Induction alimentaire de la dormance imaginale chez Semiadalia undecimnotata Schn. (Coleop. Coccinellidae) pour aider à la conservation des coccinelles élevées au laboratoire avant une utilisation ultérieure, Annales Zoologie Ecologie Animale, Volume 6 (1974)

[42] Jaquiéry, J.; Stoeckel, S.; Larose, C.; Nouhaud, P.; Rispe, C.; Mieuzet, L.; Bonhomme, J.; Mahéo, F.; Legeai, F.; Gauthier, J.-P.; Prunier-Leterme, N.; Tagu, D.; Simon, J.-C. Genetic Control of Contagious Asexuality in the Pea Aphid, PLoS Genetics, Volume 10 (2014) no. 12 | DOI

[43] JEFFS, C. T.; LEWIS, O. T. Effects of climate warming on host-parasitoid interactions, Ecological Entomology, Volume 38 (2013) no. 3, pp. 209-218 | DOI

[44] Jervis, M. A.; Ellers, J.; Harvey, J. A. Resource Acquisition, Allocation, and Utilization in Parasitoid Reproductive Strategies, Annual Review of Entomology, Volume 53 (2008) no. 1, pp. 361-385 | DOI

[45] Khodayari, S.; Moharramipour, S.; Larvor, V.; Hidalgo, K.; Renault, D. Deciphering the Metabolic Changes Associated with Diapause Syndrome and Cold Acclimation in the Two-Spotted Spider Mite Tetranychus urticae, PLoS ONE, Volume 8 (2013) no. 1 | DOI

[46] Kroon, A.; Veenendaal, R. L.; Bruin, J.; Egas, M.; Sabelis, M. W. “Sleeping with the enemy”—predator-induced diapause in a mite, Naturwissenschaften, Volume 95 (2008) no. 12, pp. 1195-1198 | DOI

[47] Lalonde, R. G. Some dynamical consequences of parasitoid diapause, Oikos, Volume 107 (2004) no. 2, pp. 338-344 | DOI

[48] Lamb, R.; Pointing, P. Sexual morph determination in the aphid, Acyrthosiphon pisum, Journal of Insect Physiology, Volume 18 (1972) no. 10, pp. 2029-2042 | DOI

[49] Langer, A.; Hance, T. Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae), Journal of Insect Physiology, Volume 46 (2000) no. 5, pp. 671-676 | DOI

[50] Le Trionnaire, G.; Francis, F.; Jaubert-Possamai, S.; Bonhomme, J.; De Pauw, E.; Gauthier, J.-P.; Haubruge, E.; Legeai, F.; Prunier-Leterme, N.; Simon, J.-C.; Tanguy, S.; Tagu, D. Transcriptomic and proteomic analyses of seasonal photoperiodism in the pea aphid, BMC Genomics, Volume 10 (2009) no. 1 | DOI

[51] Trionnaire, G.; Hardie, J.; Jaubert-Possamai, S.; Simon, J.-C.; Tagu, D. Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects, Biology of the Cell, Volume 100 (2008) no. 8, pp. 441-451 | DOI

[52] Leather, S. R. Aspects of Aphid Overwintering (Homoptera: Aphidinea: Aphididae), Entomologia Generalis, Volume 17 (1992) no. 2, pp. 101-113 | DOI

[53] Leather, S. R.; Walters, K. F. A.; Bale, J. S. The Ecology of Insect Overwintering, Cambridge University Press, 1993 | DOI

[54] POLGAR, L. Induction of dormancy in aphid parasitoids: implications for enhancing their field effectiveness, Agriculture, Ecosystems & Environment, Volume 52 (1995) no. 1, pp. 19-23 | DOI

[55] Polgar, L.; Hardie, J. Diapause induction in aphid parasitoids, Entomologia Experimentalis et Applicata, Volume 97 (2000) no. 1, pp. 21-27 | DOI

[56] Polgár, L.; Mackauer, M.; Völkl, W. Diapause induction in two species of aphid parasitoids: The influence of aphid morph, Journal of Insect Physiology, Volume 37 (1991) no. 9, pp. 699-702 | DOI

[57] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria., 2017

[58] SAYAH, F. Changes in the lipid and fatty acid composition of hemolymph and ovaries during the reproductive cycle of Labidura riparia, Entomological Science, Volume 11 (2008) no. 1, pp. 55-63 | DOI

[59] Sgrò, C. M.; Terblanche, J. S.; Hoffmann, A. A. What Can Plasticity Contribute to Insect Responses to Climate Change?, Annual Review of Entomology, Volume 61 (2016) no. 1, pp. 433-451 | DOI

[60] Sinclair, B. J.; Marshall, K. E. The many roles of fats in overwintering insects, Journal of Experimental Biology, Volume 221 (2018) | DOI

[61] Slusarczyk, M. Predator-Induced Diapause in Daphnia, Ecology, Volume 76 (1995) no. 3, pp. 1008-1013 | DOI

[62] Ślusarczyk, M. Predator-induced diapause in Daphnia magna may require two chemical cues, Oecologia, Volume 119 (1999) no. 2, pp. 159-165 | DOI

[63] Sömme, L. Mannitol and glycerol in overwintering aphid eggs, Norsk Entomologisk Tidsskrift, Volume 16 (1969)

[64] Storey, K. B.; Storey, J. M. Biochemistry of Cryoprotectants, Insects at Low Temperature, Springer US, Boston, MA, 1991, pp. 64-93 | DOI

[65] Tauber, M. J.; Tauber, C. A.; Masaki, S. Seasonal adaptations of insects, Oxford university press, New-York, USA, 1986

[66] Terblanche, J.; Klok, C.; Chown, S. Metabolic rate variation in Glossina pallidipes (Diptera: Glossinidae): gender, ageing and repeatability, Journal of Insect Physiology, Volume 50 (2004) no. 5, pp. 419-428 | DOI

[67] Teulier, L.; Weber, J.-M.; Crevier, J.; Darveau, C.-A. Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans, Proceedings of the Royal Society B: Biological Sciences, Volume 283 (2016) no. 1834 | DOI

[68] Thompson, J. N. VARIATION IN INTERSPECIFIC INTERACTIONS, Annual Review of Ecology and Systematics, Volume 19 (1988) no. 1, pp. 65-87 | DOI

[69] Tougeron, K.; Hraoui, G.; Le Lann, C.; van Baaren, J.; Brodeur, J. Intraspecific maternal competition induces summer diapause in insect parasitoids, Insect Science, Volume 25 (2017) no. 6, pp. 1080-1088 | DOI

[70] Tougeron, K.; Le Lann, C.; Brodeur, J.; van Baaren, J. Are aphid parasitoids from mild winter climates losing their winter diapause?, Oecologia, Volume 183 (2017) no. 3, pp. 619-629 | DOI

[71] Tougeron, K.; van Baaren, J.; Llopis, S.; Ridel, A.; Doyon, J.; Brodeur, J.; Le Lann, C. Disentangling plasticity from local adaptation in diapause expression in parasitoid wasps from contrasting thermal environments: a reciprocal translocation experiment, Biological Journal of the Linnean Society, Volume 124 (2018) no. 4, pp. 756-764 | DOI

[72] Tylianakis, J. M.; Didham, R. K.; Bascompte, J.; Wardle, D. A. Global change and species interactions in terrestrial ecosystems, Ecology Letters, Volume 11 (2008) no. 12, pp. 1351-1363 | DOI

[73] Vieira, R.; Míguez, J. M.; Aldegunde, M. GABA modulates day–night variation in melatonin levels in the cerebral ganglia of the damselfly Ischnura graellsii and the grasshopper Oedipoda caerulescens, Neuroscience Letters, Volume 376 (2005) no. 2, pp. 111-115 | DOI

[74] Walther, G.-R. Community and ecosystem responses to recent climate change, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 365 (2010) no. 1549, pp. 2019-2024 | DOI

[75] Boivin, G.; Martel, V. Size-induced reproductive constraints in an egg parasitoid, Journal of Insect Physiology, Volume 58 (2012) no. 12, pp. 1694-1700 | DOI

[76] Damien, M.; Tougeron, K. Prey–predator phenological mismatch under climate change, Current Opinion in Insect Science, Volume 35 (2019), pp. 60-68 | DOI

[77] IZZO, V. M.; ARMSTRONG, J.; HAWTHORNE, D.; CHEN, Y. Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore,Leptinotarsa decemlineata, Ecological Entomology, Volume 39 (2014) no. 1, pp. 75-82 | DOI

[78] Klarner, B.; Ehnes, R. B.; Erdmann, G.; Eitzinger, B.; Pollierer, M. M.; Maraun, M.; Scheu, S. Trophic shift of soil animal species with forest type as indicated by stable isotope analysis, Oikos, Volume 123 (2014) no. 10, pp. 1173-1181 | DOI

[79] Tougeron, K.; Brodeur, J.; Le Lann, C.; Baaren, J. How climate change affects the seasonal ecology of insect parasitoids, Ecological Entomology, Volume 45 (2019) no. 2, pp. 167-181 | DOI

Cited by Sources: