Geographic variation in larval cold tolerance and exposure across the invasion front of a widely established forest insect

Petra Hafker , Lily M. Thompson , Jonathan A. Walter , Dylan Parry , Kristine L. Grayson

Insect Science ›› 2024, Vol. 31 ›› Issue (6) : 1930 -1942.

PDF
Insect Science ›› 2024, Vol. 31 ›› Issue (6) : 1930 -1942. DOI: 10.1002/1744-7917.13358
ORIGINAL ARTICLE

Geographic variation in larval cold tolerance and exposure across the invasion front of a widely established forest insect

Author information +
History +
PDF

Abstract

Under global climate change, high and low temperature extremes can drive shifts in species distributions. Across the range of a species, thermal tolerance is based on acclimatization, plasticity, and may undergo selection, shaping resilience to temperature stress. In this study, we measured variation in cold temperature tolerance of early instar larvae of an invasive forest insect,  Lymantria dispar dispar L. (Lepidoptera: Erebidae), using populations sourced from a range of climates within the current introduced range in the Eastern United States. We tested for population differences in chill coma recovery (CCR) by measuring recovery time following a period of exposure to a nonlethal cold temperature in 2 cold exposure experiments. A 3rd experiment quantified growth responses after CCR to evaluate sublethal effects. Our results indicate that cold tolerance is linked to regional climate, with individuals from populations sourced from colder climates recovering faster from chill coma. While this geographic gradient is seen in many species, detecting this pattern is notable for an introduced species founded from a single point-source introduction. We demonstrate that the cold temperatures used in our experiments occur in nature during cold spells after spring egg hatch, but impacts to growth and survival appear low. We expect that population differences in cold temperature performance manifest more from differences in temperature-dependent growth than acute exposure. Evaluating intraspecific variation in cold tolerance increases our understanding of the role of climatic gradients on the physiology of an invasive species, and contributes to tools for predicting further expansion.

Keywords

chill coma recovery / forest insect / geographic gradient / Lymantria dispar / spring cold spell / thermal performance

Cite this article

Download citation ▾
Petra Hafker, Lily M. Thompson, Jonathan A. Walter, Dylan Parry, Kristine L. Grayson. Geographic variation in larval cold tolerance and exposure across the invasion front of a widely established forest insect. Insect Science, 2024, 31(6): 1930-1942 DOI:10.1002/1744-7917.13358

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ayrinhac, A.,Debat, V.,Gibert, P.,Kister, A.G.,Legout, H.,Moreteau, B. et al. (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Functional Ecology,18,700–706.

[2]

Banahene, N.,Salem, S.K.,Faske, T.M.,Byrne, H.M.,Glackin, M.,Agosta, S.J. et al. (2018) Thermal sensitivity of gypsy moth (Lepidoptera: Erebidae) during larval and pupal development. Environmental Entomology,47,1623–1631.

[3]

Butterson, S.,Roe, A.D. and Marshall, K.E. (2021) Plasticity of cold hardiness in the eastern spruce budworm,Choristoneura fumiferana. Comparative Biochemistry and Physiology, Part A. Molecular & Integrative Physiology,259,110998.

[4]

Castañeda, L.E.,Lardies, M.A. and Bozinovic, F. (2005) Interpopulational variation in recovery time from chill coma along a geographic gradient: a study in the common woodlouse,Porcellio laevis. Journal of Insect Physiology,51,1346–1351.

[5]

Clark, K.L.,Skowronski, N. and Hom, J. (2010) Invasive insects impact forest carbon dynamics. Global Change Biology,16,88–101.

[6]

Cohen, J.,Screen, J.A.,Furtado, J.C.,Barlow, M.,Whittleston, D.,Coumou, D. et al. (2014) Recent arctic amplification and extreme mid-latitude weather. Nature Geoscience,7,627–637.

[7]

David, R.J.,Gibert, P.,Moreteau, B.,Gilchrist, G.W. and Huey, R.B. (2003) The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Functional Ecology,17,425–430.

[8]

David, R.J.,Gibert, P.,Pla, E.,Petavy, G.,Karan, D. and Moreteau, B. (1998) Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology,23,291–299.

[9]

Doane, C.C. and McManus, M.L. (1981) The Gypsy Moth: Research Toward Integrated Pest Management. Washington, D.C.: U.S. Department of Agriculture.

[10]

Elkinton, J.S. and Liebhold, A.M. (1990) Population dynamics of gypsy moth in North America. Annual Review of Entomology,35,571–596.

[11]

Erelli, M.C. and Elkinton, J.S. (2000) Maternal effects on gypsy moth (Lepidoptera: Lymantriidae) population dynamics: a field experiment. Environmental Entomology,29,476–488.

[12]

Faske, T.M.,Thompson, L.M.,Banahene, N.,Levorse, A.,Quiroga Herrera, M.,Sherman, K. et al. (2019) Can gypsy moth stand the heat? a reciprocal transplant experiment with an invasive forest pest across its southern range margin. Biological Invasions,21,1365–1378.

[13]

Forrest, J.R. (2016) Complex responses of insect phenology to climate change. Current Opinion in Insect Science,17,49–54.

[14]

Friedline, C.J.,Faske, T.M.,Lind, B.M.,Hobson, E.M.,Parry, D.,Dyer, R.J. et al. (2019) Evolutionary genomics of gypsy moth populations sampled along a latitudinal gradient. Molecular Ecology,28,2206–2223.

[15]

Garcia, M.J.,Littler, A.S.,Sriram, A. and Teets, N.M. (2020) Distinct cold tolerance traits independently vary across genotypes in Drosophila melanogaster. Evolution; International Journal of Organic Evolution,74,1437–1450.

[16]

Gerken, A.R.,Mackay, T.F.C. and Morgan, T.J. (2016) Artificial selection on chill-coma recovery time in Drosophila melanogaster: direct and correlated responses to selection. Journal of Thermal Biology,59,77–85.

[17]

Gibert, P. and Huey, R.B. (2001) Chill-coma temperature in Drosophila: effects of developmental temperature, latitude, and phylogeny. Physiological and Biochemical Zoology,74,429–434.

[18]

Gibert, P.,Moreteau, B.,Pétavy, G.,Karan, D. and David, J.R. (2001) Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution; International Journal of Organic Evolution,55,1063–1068.

[19]

Gray, D.R. (2009) Age-dependent postdiapause development in the gypsy moth (Lepidoptera: Lymantriidae) life stage model. Environmental Entomology,38,18–25.

[20]

Gray, D.R. (2004) . The gypsy moth life stage model: landscape-wide estimates of gypsy moth establishment using a multi-generational phenology model. Ecological Modelling,176,155–171.

[21]

Hoffmann, A.A.,Anderson, A. and Hallas, R. (2002) Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecology Letters,5,614–618.

[22]

Huey, R.B. and Hertz, P.E. (1984) Is a jack-of-all-temperatures a master of none? Evolution; International Journal of Organic Evolution,38,441–444.

[23]

Hufkens, K.,Basler, D.,Milliman, T.,Melaas, E.K. and Richardson, A.D. (2018) An integrated phenology modelling framework in R. Methods in Ecology and Evolution,9,1276–1285.

[24]

Jactel, H.,Koricheva, J. and Castagneyrol, B. (2019) Responses of forest insect pests to climate change: not so simple. Current Opinion in Insect Science,35,103–108.

[25]

Kindlmann, P.,Dixon, A.F.G. and Dostálková I. (2001) Role of ageing and temperature in shaping reaction norms and fecundity functions in insects. Journal of Evolutionary Biology,14,835–840.

[26]

Kleynhans, E.,Mitchell, K.A.,Conlong, D.E. and Terblanche, J.S. (2014) Evolved variation in cold tolerance among populations of Eldana saccharina (Lepidoptera: Pyralidae) in South Africa. Journal of Evolutionary Biology,27,1149–1159.

[27]

Klock, C.J. and Chown, S.L. (2003) Resistance to temperature extremes in sub-Antarctic weevils: interspecific variation, population differentiation and acclimation. Biological Journal of the Linnean Society,78,401–414.

[28]

Kretschmer, M.,Coumou, D.,Agel, L.,Barlow, M.,Tziperman, E. and Cohen, J. (2018) More-persistent weak stratospheric polar vortex states linked to cold extremes. Bulletin of the American Meteorological Society,99,49–60.

[29]

Lancaster, L.T. (2016) Widespread range expansions shape latitudinal variation in insect thermal limits. Nature Climate Change,6,618–621.

[30]

Lawrence, D.M. and Slater, A.G. (2010) The contribution of snow condition trends to future ground climate. Climate Dynamics,34,969–981.

[31]

Liebhold, A.M. (1995) Suitability of North American Tree Species to the Gypsy Moth: A Summary of Field and Laboratory Tests. Radnor, PA: U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station.

[32]

MacLean, H.J.,Sørensen, J.G.,Kristensen, T.N.,Loeschcke, V.,Beedholm, K.,Kellermann, V. et al. (2019) Evolution and plasticity of thermal performance: an analysis of variation in thermal tolerance and fitness in 22 Drosophila species. Philosophical Transactions of the Royal Society B: Biological Sciences,374,20180548.

[33]

MacMillan, H.A. and Sinclair, B.J. (2011) Mechanisms underlying insect chill-coma. Journal of Insect Physiology,57,12–20.

[34]

MacQuarrie, C.J.K., Cooke, B.J. and Saint-Amant, R. (2019) The predicted effect of the polar vortex of 2019 on winter survival of emerald ash borer and mountain pine beetle. Canadian Journal of Forest Research,49,1165–1172.

[35]

Marshall, K.E.,Gotthard, K. and Williams, C.M. (2020) Evolutionary impacts of winter climate change on insects. Current Opinion in Insect Science,41,54–62.

[36]

Morgan, T.J. and Mackay, T.F.C. (2006) Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity,96,232–242.

[37]

Pang, X.,Zhang, J.,Han, Y.,Sun, L. and Cao, C. (2022) Functional characterization of a diuretic hormone receptor associated with desiccation, starvation and temperature tolerance in gypsy moth,Lymantria dispar. Pesticide Biochemistry and Physiology,184,105079.

[38]

PRISM Climate Group, Oregon State University, 30-Year Normals 1981–2010. data created 11 July 2012. Available from: https://prism.oregonstate.edu [Accessed 7th November 2018]

[39]

Pureswaran, D.S.,Roques, A. and Battisti, A. (2018) Forest insects and climate change. Current Forestry Reports,4,35–50.

[40]

Roland, J. and Matter, S.F. (2016) Pivotal effect of early-winter temperatures and snowfall on population growth of alpine Parnassius smintheus butterflies. Ecological Monographs,86,412–428.

[41]

Rossiter, M.C.,Cox-Foster, D.L. and Briggs, M.A. (1993) Initiation of maternal effects in Lymantria dispar: genetic and ecological components of egg provisioning. Journal of Evolutionary Biology,6,577–589.

[42]

Sharov, A.A.,Leonard, D.,Liebhold, A.M.,Roberts, E.A. and Dickerson, W. (2002) “Slow the Spread”: a national program to contain the gypsy moth. Journal of Forestry,100,30–36.

[43]

Sinclair, B.J.,Alvarado, L.E.C. and Ferguson, L.V. (2015) An invitation to measure insect cold tolerance: methods, approaches, and workflow. Journal of Thermal Biology,53,180–197.

[44]

Sinclair, B.J. and Roberts, S.P. (2005) Acclimation, shock and hardening in the cold. Journal of Thermal Biology,30,557–562.

[45]

Sinclair, B.J.,Williams, C.M. and Terblanche, J.S. (2012) Variation in thermal performance among insect populations. Physiological and Biochemical Zoology,85,594–606.

[46]

Sisodia, S. and Singh, B.N. (2010) Influence of developmental temperature on cold shock and chill coma recovery in Drosophila ananassae: acclimation and latitudinal variations among Indian populations. Journal of Thermal Biology,35,117–124.

[47]

Streifel, M.A.,Tobin, P.C.,Kees, A.M. and Aukema, B.H. (2019) Range expansion of Lymantria dispar dispar (L.) (Lepidoptera: Erebidae) along its north-western margin in North America despite low predicted climatic suitability. Journal of Biogeography,46,58–69.

[48]

Thompson, L.M.,Faske, T.M.,Banahene, N.,Grim, D.,Agosta, S.J.,Parry, D. et al. (2017) Variation in growth and developmental responses to supraoptimal temperatures near latitudinal range limits of gypsy moth Lymantria dispar (L.), an expanding invasive species. Physiological Entomology,42,181–190.

[49]

Thompson, L.M.,Powers, S.D.,Appolon, A.,Hafker, P.,Milner, L.,Parry, D. et al. (2021) Climate-related geographical variation in performance traits across the invasion front of a widespread non-native insect. Journal of Biogeography,48,405–414.

[50]

Thornton, M.M.,Shrestha, R.,Wei, Y.,Thornton, P.E.,Kao, S.C. and Wilson, B.E. (2020) Daymet: Daily Surface Weather Data on a 1-km Grid for North America, Version 4. ORNL DAAC,Oak Ridge, Tennessee, USA. Available from:

[51]

Tobin, P.C.,Cremers, K.T.,Hunt, L. and Parry, D. (2016) All quiet on the western front? Using phenological inference to detect the presence of a latent gypsy moth invasion in northern Minnesota. Biological Invasions,18,3561–3573.

[52]

Vavrus, S.,Walsh, J.E.,Chapman, W.L. and Portis, D. (2006) The behavior of extreme cold air outbreaks under greenhouse warming. International Journal of Climatology,26,1133–1147.

[53]

Williams, C.M.,Henry, H.A.L. and Sinclair, B.J. (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biological Reviews,90,214–235.

[54]

Wu, Y.,Molongoski, J.J.,Winograd, D.F.,Bogdanowicz, S.M.,Louyakis, A.S.,Lance, D.R. et al. (2015) Genetic structure, admixture and invasion success in a Holarctic defoliator, the gypsy moth (Lymantria dispar, Lepidoptera: Erebidae). Molecular Ecology,24,1275–1291.

[55]

Yang, L.H.,Postema, E.G.,Hayes, T.E.,Lippey, M.K. and MacArthur-Waltz, D.J. (2021) The complexity of global change and its effects on insects. Current Opinion in Insect Science,47,90–102.

[56]

Zachariassen, K.E. (1985) Physiology of cold tolerance in insects. Physiological Reviews,65,799–832.

RIGHTS & PERMISSIONS

2024 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

199

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/