Skip to main content

Advertisement

Log in

Measuring the evolutionary potential of a winter-active parasitic wasp to climate change

  • Physiological ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

In temperate climates, as a consequence of warming winters, an increasing number of ectothermic species are remaining active throughout winter months instead of diapausing, rendering them increasingly vulnerable to unpredictable cold events. One species displaying a shift in overwintering strategy is the parasitoid wasp and biological control agent Aphidius avenae. The current study aimed to better understand the consequence of a changing overwintering strategy on the evolutionary potential of an insect population to adapt to the cold stress events, set to increase in frequency, even during milder winters. Using a parental half-sibling breeding design, narrow-sense heritability of the cold tolerance, morphology and longevity of A. avenae was estimated. The heritability of cold tolerance was estimated at 0.07 (CI95% = [0.00; 0.25]) for the Critical Thermal Minima (CTmin) and 0.11 (CI95% = [0.00; 0.34]) for chill coma temperature; estimates much lower than those obtained for morphological traits (tibia length 0.20 (CI95% = [0.03; 0.37]); head width 0.23 (CI95% = [0.09; 0.39]); wing surface area 0.28 (CI95% = [0.11; 0.47])), although comparable with the heritability estimate of 0.12 obtained for longevity (CI95% = [0.00; 0.25]). The heritability estimates obtained thus suggest that A. avenae possesses low adaptive potential against cold stress. If such estimates are indicative of the evolutionary potential of A. avenae cold tolerance, more emphasis may be placed on adaptive phenotypic plasticity at the individual level to persist in a changing climate, with potential implications for the biological control function they provide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • IPCC (2013) Climate change 2013 the physical science basis: Final draft underlying scientific-technical assessment?: Working Group I Contribution to the IPCC Fifth Assessment Report (ed. by TF Stocker, D Qin, G-K. Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex and PM Midgley). Cambridge University Press, Cambridge, UK and New York, NY

  • Alford L, Kishani Farahani H, Pierre JS, Burel F, van Baaren J (2017) Why is there no impact of the host species on the cold tolerance of a generalist parasitoid? J Insect Physiol 103:71–77

    CAS  PubMed  Google Scholar 

  • Alford L, Tougeron K, Pierre J-S, Burel F, van Baaren J (2018) The effect of landscape complexity and microclimate on the thermal tolerance of a pest insect. Insect Sci 25:905–915

    PubMed  Google Scholar 

  • Andersen JL, Manenti T, Sørensen JG, MacMillan HA, Loeschcke V, Overgaard J (2015) How to assess Drosophila cold tolerance: chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Funct Ecol 29:55–65

    Google Scholar 

  • Andrade TO, Herve M, Outreman Y, Krespi L, van Baaren J (2013) Winter host exploitation influences fitness traits in a parasitoid. Entomol Exp Appl 147:167–174

    Google Scholar 

  • Andrade TO, Outreman Y, Krespi L, Plantegenest M, Vialatte A, Gauffre B, van Baaren J (2015) Spatiotemporal variations in aphid-parasitoid relative abundance patterns and food webs in agricultural ecosystems. Ecosphere 6:113

    Google Scholar 

  • Andrade TO, Krespi L, Bonnardot V, van Baaren J, Outreman Y (2016) Impact of change in winter strategy of one parasitoid species on the diversity and function of a guild of parasitoids. Oecologia 180:877–888

    PubMed  Google Scholar 

  • Andrew NR, Hart RA, Jung M-P, Hemmings Z, Terblanche JS (2013) Can temperate insects take the heat? A case study of the physiological and behavioural responses in a common ant, Iridomyrmex purpureus (Formicidae), with potential climate change. J Insect Physiol 59:870–880

    CAS  PubMed  Google Scholar 

  • Arnett AE, Gotelli NJ (2003) Bergmann’s rule in larval ant lions: testing the starvation resistance hypothesis. Ecol Entomol 28:645–650

    Google Scholar 

  • Bale JS (1996) Insect cold hardiness: a matter of life and death. Eur J Entomol 93:369–382

    Google Scholar 

  • Bale JS, Hayward SAL (2010) Insects overwintering in a changing climate. J Exp Biol 213:980–994

    CAS  PubMed  Google Scholar 

  • Bentz BJ, Powell JA (2014) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am Nat 184:787–796

    PubMed  Google Scholar 

  • Blanckenhorn WU, Fanti J, Reim C (2007) Size-dependent energy reserves, energy utilization and longevity in the yellow dung fly. Physiol Entomol 32:372–381

    Google Scholar 

  • Chown SL, Jumbam KR, Sørensen JG, Terblanche JS (2009) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct Ecol 23:133–140

    Google Scholar 

  • Christiansen-Weniger P, Hardie J (1997) 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 42:165–172

    Google Scholar 

  • Christiansen-Weniger P, Hardie J (1999) Environmental and physiological factors for diapause induction and termination in the aphid parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae). J Insect Physiol 45:357–364

    CAS  PubMed  Google Scholar 

  • Cushman JH, Lawton JH, Manly BF (1993) Latitudinal patterns in European ant assemblages: variation in species richness and body size. Oecologia 95:30–37

    PubMed  Google Scholar 

  • Damien M, Le Lann C, Desneux N, Alford L, Al Hassan D, Georges R, van Baaren J (2017) Floral resource increases winter pest control but not trophic link diversity. Agric Ecosyst Environ 247:418–424

    Google Scholar 

  • de Jong MA, Saastamoinen M (2018) Environmental and genetic control of cold tolerance in the Glanville fritillary butterfly. J Evol Biol 31:636–645

    PubMed  PubMed Central  Google Scholar 

  • de Jong MA, Collins S, Beldade P, Brakefield PM, Zwaan BJ (2013) Footprints of selection in wild populations of Bicyclus anynana along a latitudinal cline. Mol Ecol 22:341–353

    PubMed  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Ann Rev Entomol 47:93–122

    CAS  Google Scholar 

  • Diffenbaugh NS, Field CB (2013) Changes in ecologically critical terrestrial climate conditions. Science 341:486–492

    CAS  PubMed  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074

    CAS  PubMed  Google Scholar 

  • Eoche-Bosy D, Outreman Y, Andrade TO, Krespi L, van Baaren J (2016) Seasonal variations in the availability of host resources influence foraging strategy in parasitoids. Entomol Exp Appl 16:11–19

    Google Scholar 

  • Franks SJ, Hoffmann AA (2012) Genetics of climate change. Annu Rev Genet 46:185–208

    CAS  PubMed  Google Scholar 

  • Frydenberg J, Hoffmann AA, Loeschcke V (2003) DNA sequence variation and latitudinal associations in hsp23, hsp26 and hsp27 from natural populations of Drosophila melanogaster. Mol Ecol 12:2025–2032

    CAS  PubMed  Google Scholar 

  • Gerken AR, Eller OC, Hahn DA, Morgan TJ (2015) Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. Proc Natl Acad Sci USA 112:4399–4404

    CAS  PubMed  Google Scholar 

  • Gilchrist GW, Huey RB (1999) The direct response of Drosophila melanogaster to selection on knockdown temperature. Heredity 83:15–29

    PubMed  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B 282:20150401

    PubMed  Google Scholar 

  • Harrington R, Taylor LR (1990) Migration for survival—fine-scale population redistribution in an aphid, Myzus persicae. J Anim Ecol 59:1177–1193

    Google Scholar 

  • Hazell SP, Bale JS (2011) Low temperature thresholds: are chill coma and CT(min) synonymous? J Insect Physiol 57:1085–1089

    CAS  PubMed  Google Scholar 

  • Huey RB, Crill WD, Kingsolver JG, Weber KE (1992) A method for rapid measurement of heat or cold resistance of small insects. Funct Ecol 6:489–494

    Google Scholar 

  • Hughes GE, Owen E, Bale JS, Sterk G (2010) Thermal activity thresholds of the parasitic wasp Lysiphlebus testaceipes and its aphid prey: implications for the efficacy of biological control. Physiol Entomol 35:373–378

    Google Scholar 

  • Ismail M, Vernon P, Hance T, Pierre J-S, van Baaren J (2012) What are the possible benefits of small size for energy constrained ectotherms in cold stress conditions? Oikos 121:2072–2080

    Google Scholar 

  • Kellermann V, van Heerwaarden B, Sgro CM, Hoffmann AA (2009) Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325:1244–1246

    CAS  PubMed  Google Scholar 

  • Kunkel KE, Pielke RAJ, Changnon SA (1999) Temporal fluctuations in weather and climate extremes that cause economic and human health impacts: a review. Bull Am Meteorol Soc 80:1077–1098

    Google Scholar 

  • Le Lann C, Roux O, Serain N, van Alphen JJM, Vernon P, van Baaren J (2011) Thermal tolerance of sympatric hymenopteran parasitoid species: does it match seasonal activity? Physiol Entomol 36:21–28

    Google Scholar 

  • May ML (1979) Insect thermoregulation. Annu Rev Entomol 24:313–349

    Google Scholar 

  • Ma F-Z, Lü Z-C, Wang R, Wan F-H (2014) Heritability and evolutionary potential in thermal tolerance traits in the invasive Mediterranean cryptic species of Bemisia tabaci (Hemiptera: Aleyrodidae). PLoS ONE 9:e103279

    PubMed  PubMed Central  Google Scholar 

  • McColl G, Hoffmann AA, McKechnie SW (1996) Response of two heat shock genes to selection for knockdown heat resistance in Drosophila melanogaster. Genetics 143:1615–1627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell KA, Hoffmann AA (2010) Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila. Funct Ecol 24:694–700

    Google Scholar 

  • Morgan TJ, Mackay TF (2006) Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96:232–242

    CAS  PubMed  Google Scholar 

  • Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:187–208

    CAS  PubMed  Google Scholar 

  • Paull SH, Johnson PTJ (2014) Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecol Lett 17:445–453

    PubMed  Google Scholar 

  • Powell SJ, Bale JS (2004) Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: aphididae). J Insect Physiol 50:277–284

    CAS  PubMed  Google Scholar 

  • Powell SJ, Bale JS (2005) Low temperature acclimated populations of the grain aphid Sitobion avenae retain ability to rapidly cold harden with enhanced fitness. J Exp Biol 208:2615–2620

    CAS  PubMed  Google Scholar 

  • Powell SJ, Bale JS (2006) Effect of long-term and rapid cold hardening on the cold torpor temperature of an aphid. Physiol Entomol 31:348–352

    Google Scholar 

  • Rezende EL, Tejedo M, Santos M (2011) Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Funct Ecol 25:111–121

    Google Scholar 

  • Roff D (2003) Evolution: evolutionary danger for rainforest species. Science 301:58–59

    CAS  PubMed  Google Scholar 

  • Rolandi C, Lighton JRB, de la Vega GJ, Schilman PE, Mensch J (2018) Genetic variation for tolerance to high temperatures in a population of Drosophila melanogaster. Ecol Evol 8:10374–10383

    PubMed  PubMed Central  Google Scholar 

  • Roux O, Le Lann C, van Alphen JJM, van Baaren J (2010) How does heat shock affect the life history traits of adults and progeny of the aphid parasitoid Aphidius avenae (Hymenoptera: Aphidiidae)? Bull Entomol Res 100:543–549

    CAS  PubMed  Google Scholar 

  • Salin C, Deprez B, Van Bockstaele DR, Mahillon J, Hance T (2004) Sex determination mechanism in the hymenopteran parasitoid Aphidius rhopalosiphi De Stefani-Peres (Braconidae: Aphidiinae). Belg J Zool 134:15–21

    Google Scholar 

  • Schurch R, Accleton C, Field J (2016) Consequences of a warming climate for social organisation in sweat bees. Behav Ecol Sociobiol 70:1131–1139

    PubMed  PubMed Central  Google Scholar 

  • Sgrò CM, Terblanche JS, Hoffmann AA (2016) What can plasticity contribute to insect responses to climate change? Annu Rev Entomol 61:433–451

    PubMed  Google Scholar 

  • Sinclair BJ (2003) Field ecology of freeze tolerance: interannual variation in cooling rates, freeze-thaw and thermal stress in the microhabitat of the alpine cockroach Celatoblatta quinquemaculata. Oikos 93:286–293

    Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Google Scholar 

  • Stuhldreher G, Hermann G, Fartmann T (2014) Cold-adapted species in a warming world—an explorative study on the impact of high winter temperatures on a continental butterfly. Entomol Exp Appl 151:270–279

    Google Scholar 

  • Terblanche JS, Deere JA, Clusella Trullas S, Janion C, Chown SL (2007) Critical thermal limits depend on methodological context. Proc R Soc Lond B 274:2935–2942

    Google Scholar 

  • Terblanche JS, Hoffmann AA, Mitchell KA, Rako L, le Roux PC, Chown SL (2011) Ecologically relevant measures of tolerance to potentially lethal temperatures. J Exp Biol 214(22):3713–3725

    PubMed  Google Scholar 

  • Tougeron K, van Baaren J, Burel F, Alford L (2016) Comparing thermal tolerance across contrasting landscapes: first steps towards understanding how landscape management could modify ectotherm thermal tolerance. Insect Conserv Divers 9:171–180

    Google Scholar 

  • Tougeron K, Le Lann C, Brodeur J, van Baaren J (2017) Are aphid parasitoids from mild winter climates losing their winter diapause? Oecologia 183:619–629

    PubMed  Google Scholar 

  • Weber KE, Diggins LT (1990) Increased selection response in larger populations. II. Selection for ethanol vapour resistance in Drosophila melanogaster at two population sizes. Genetics 125:585–597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90:214–235

    PubMed  Google Scholar 

  • Zhao C, Ma F, Chen H, Wan F, Guo J, Zhou Z (2018) Heritability and evolutionary potential drive cold hardiness in the overwintering Ophraella communa beetles. Front Physiol 9:666

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge Stephanie Llopis and Charlotte Alford for assistance with morphological measurements, and Annabelle Androdias, Cécile Carré, Kévin Tougeron and Thomas Franco for assistance with parasitoid mating.

Funding

This study was funded by a Marie Skłodowska-Curie Actions Intra-European Fellowship for the project ‘Climland’ (FP7-PEOPLE-2012-IEF-326943) and an Individual Fellowship for the project ‘FAB’ (H2020-MSCA-IF-2018-841952).

Author information

Authors and Affiliations

Authors

Contributions

PL and JvB designed the study. Data collection was performed by PL and LA and data analysis by FM and PL. The first draft of the manuscript was written by LA and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lucy Alford.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Roland Brandl.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alford, L., Louâpre, P., Mougel, F. et al. Measuring the evolutionary potential of a winter-active parasitic wasp to climate change. Oecologia 194, 41–50 (2020). https://doi.org/10.1007/s00442-020-04761-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-020-04761-2

Keywords

Navigation