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Geographic divergence in upper thermal limits across insect life stages: does behavior matter?

Abstract

Insects with complex life cycles vary in size, mobility, and thermal ecology across life stages. We examine how differences in the capacity for thermoregulatory behavior influence geographic differences in physiological heat tolerance among egg and adult Colias butterflies. Colias adults exhibit differences in morphology (wing melanin and thoracic setal length) along spatial gradients, whereas eggs are morphologically indistinguishable. Here we compare Colias eriphyle eggs and adults from two elevations and Colias meadii from a high elevation. Hatching success and egg development time of C. eriphyle eggs did not differ significantly with the elevation of origin. Egg survival declined in response to heat-shock temperatures above 38–40 °C and egg development time was shortest at intermediate heat-shock temperatures of 33–38 °C. Laboratory experiments with adults showed survival in response to heat shock was significantly greater for Colias from higher than from lower elevation sites. Common-garden experiments at the low-elevation field site showed that C. meadii adults initiated heat-avoidance and over-heating behaviors significantly earlier in the day than C. eriphyle. Our study demonstrates the importance of examining thermal tolerances across life stages. Our findings are inconsistent with the hypothesis that thermoregulatory behavior inhibits the geographic divergence of physiological traits in mobile stages, and suggest that sessile stages may evolve similar heat tolerances in different environments due to microclimatic variability or evolutionary constraints.

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References

  1. Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc Lond Ser B 267:739–745. doi:10.1098/rspb.2000.1065

    CAS  Article  Google Scholar 

  2. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  3. Angilletta MJ, Zelic MH, Adrian GJ, Hurliman AM, Smith CD (2013) Heat tolerance during embryonic development has not diverged among populations of a widespread species (Sceloporus Undulatus). Conserv Physiol 1:cot018. doi:10.1093/conphys/cot018

    Article  Google Scholar 

  4. Bonebrake TC, Boggs CL, McNally JM, Ranganathan J, Ehrlich PR (2010) Oviposition behavior and offspring performance in herbivorous insects: consequences of climatic and habitat heterogeneity. Oikos 119:927–934. doi:10.1111/j.1600-0706.2009.17759.x

    Article  Google Scholar 

  5. Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol Rev 83:339–355. doi:10.1111/j.1469-185X.2008.00046.x

    Article  PubMed  Google Scholar 

  6. Buckley LB, Kingsolver JG (2012) The demographic impacts of shifts in climate means and extremes on alpine butterflies. Funct Ecol 26:969–977. doi:10.1111/j.1365-2435.2012.01969.x

    Article  Google Scholar 

  7. Buckley LB, Ehrenberger JC, Angilletta MJ (2015) Thermoregulatory behavior limits local adaptation of thermal niches and confers sensitivity to climate change. Funct Ecol. doi:10.1111/1365-2435.12406

    Google Scholar 

  8. Chown SL (2001) Physiological variation in insects: hierarchical levels and implications. J Insect Physiol 47:649–660. doi:10.1016/S0022-1910(00)00163-3

    CAS  Article  PubMed  Google Scholar 

  9. Diamond SE et al (2012) Who likes it hot? a global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants. Glob Change Biol 18:448–456. doi:10.1111/j.1365-2486.2011.02542.x

    Article  Google Scholar 

  10. Ellers J, Boggs CL (2004) Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies. Biol J Linn Soc 82:79–87. doi:10.1111/j.1095-8312.2004.00319.x

    Article  Google Scholar 

  11. García-Barros E (2000) Egg size in butterflies (Lepidoptera: papilionoidea and Hesperiidae): a summary of data. J Res Lepidoptera 35:90–136

    Google Scholar 

  12. Grambsch TMTaPM (2014) Modeling survival data: extending the cox model. R package version 2.37-7 http://CRAN.R-project.org/package=survival

  13. Hayes JL (1980) Some Aspects of the Biology of the Developmental Stages of Colias alexandra (Pieridae). J Lepidopterists Soc 34(4): 345–352

    Google Scholar 

  14. Hertz PE (1981) Adaptation to altitude in two West Indian Anoles (Reptilia). J Zool 195:25–37. doi:10.1111/j.1469-7998.1981.tb01891.x

    Article  Google Scholar 

  15. Higgins JK (2014) Rapid evolution and population divergence in response to environmental change in Colias butterflies. PhD, University of North Carolina at Chapel Hill, Chapel Hill

  16. Higgins JK, MacLean HJ, Buckley LB, Kingsolver JG (2014) Geographic differences and microevolutionary changes in thermal sensitivity of butterfly larvae in response to climate. Funct Ecol 28:982–989. doi:10.1111/1365-2435.12218

    Article  Google Scholar 

  17. Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. doi:10.1017/S1464793105006767

    Article  PubMed  Google Scholar 

  18. Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366. doi:10.1086/346135

    Article  PubMed  Google Scholar 

  19. IPCC, Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (2014) Ipcc climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York

  20. Kingsolver JG, Buckley LB (2015) Climate variability slows evolutionary responses of Colias butterflies to recent climate change. Proc R Soc B. doi:10.1098/rspb.2014.2470

    PubMed Central  Google Scholar 

  21. Kingsolver JG (1983) Ecological significance of flight activity in Colias butterflies: Implications for reproductive strategy and population structure. Ecol 64:545–551

    Google Scholar 

  22. Kingsolver JG, Moffat RJ (1982) Thermoregulation and the determinants of heat transfer in Colias butterflies. Oecologia 53:27–33. doi:10.1007/BF00377132

    Article  Google Scholar 

  23. Kingsolver JG, Watt WB (1984) Mechanistic constraints and optimality models: thermoregulatory strategies in Colias butterflies. Ecol 65: 1835–1839

    Article  Google Scholar 

  24. Kingsolver JG, Arthur Woods H, Buckley LB, Potter KA, MacLean HJ, Higgins JK (2011) Complex life cycles and the responses of insects to climate change. Integr Comp Biol 51:719–732. doi:10.1093/icb/icr015

    Article  PubMed  Google Scholar 

  25. Krebs RA, Loeschcke V (1995) Resistance to thermal stress in preadult Drosophila buzzatii: variation among populations and changes in relative resistance across life stages. Biol J Linn Soc 56:517–531. doi:10.1111/j.1095-8312.1995.tb01108.x

    Article  Google Scholar 

  26. Levy O et al (2015) Resolving the life cycle alters expected impacts of climate change. Proc R Soc Lond B. doi:10.1098/rspb.2015.0837

    Google Scholar 

  27. Loeschcke V, Krebs R, Dahlgaard J, Michalak P (1997) High-temperature stress and the evolution of thermal resistance in Drosophila. In: Bijlsma R, Loeschcke V (eds) Environmental stress, adaptation and evolution, vol 83. Birkhäuser, Basel, pp 175–190

    Chapter  Google Scholar 

  28. Marais E, Terblanche JS, Chown SL (2009) Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae). J Insect Physiol 55:336–343. doi:10.1016/j.jinsphys.2008.11.016

    CAS  Article  PubMed  Google Scholar 

  29. Mitchell KA, Sinclair BJ, Terblanche JS (2013) Ontogenetic variation in cold tolerance plasticity in Drosophila: is the Bogert effect bogus? Naturwissenschaften 100:281–284. doi:10.1007/s00114-013-1023-8

    CAS  Article  PubMed  Google Scholar 

  30. Pincebourde S, Woods HA (2012) Climate uncertainty on leaf surfaces: the biophysics of leaf microclimates and their consequences for leaf-dwelling organisms. Funct Ecol 26:844–853. doi:10.1111/j.1365-2435.2012.02013.x

    Article  Google Scholar 

  31. Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2014) Nlme: linear and nonlinear mixed effects models. R package version 3.1-117 http://CRAN.R-project.org/package=nlme

  32. Potter K, Davidowitz G, Woods HA (2009) Insect eggs protected from high temperatures by limited homeothermy of plant leaves. J Exp Biol 212:3448–3454. doi:10.1242/jeb.033365

    Article  PubMed  Google Scholar 

  33. Potter KA, Davidowitz G, Arthur Woods H (2011) Cross-stage consequences of egg temperature in the insect Manduca sexta. Funct Ecol 25:548–556. doi:10.1111/j.1365-2435.2010.01807.x

    Article  Google Scholar 

  34. Potter KA, Arthur Woods H, Pincebourde S (2013) Microclimatic challenges in global change biology. Glob Change Biol 19:2932–2939. doi:10.1111/gcb.12257

    Article  Google Scholar 

  35. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  36. Radchuk V, Turlure C, Schtickzelle N (2013) Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J Anim Ecol 82:275–285. doi:10.1111/j.1365-2656.2012.02029.x

    Article  PubMed  Google Scholar 

  37. Rawlins JE (1980) Thermoregulation by the black swallowtail butterfly, Papilio Polyxenes (Lepidoptera: Papilionidae). Ecology. doi:10.2307/1935193

    Google Scholar 

  38. Sarup P, Sørensen JG, Dimitrov K, Barker J, Loeschcke V (2006) Climatic adaptation of Drosophila buzzatii populations in Southeast Australia. Heredity 96:479–486. doi:10.1038/sj.hdy.6800828

    CAS  Article  PubMed  Google Scholar 

  39. Sherman PW, Watt WB (1973) The thermal ecology of some Colias butterfly larvae. J Comp Physiol 83:25–40. doi:10.1007/BF00694570

    Article  Google Scholar 

  40. Shirai Y (2000) Temperature tolerance of the diamondback moth, Plutella Xylostella (Lepidoptera: Yponomeutidae) in tropical and temperate regions of Asia. Bull Entomol Res 90:357–364. doi:10.1017/S0007485300000481

    CAS  PubMed  Google Scholar 

  41. Sinclair BJ, Ferguson LV, Salehipour-shirazi G, MacMillan HA (2013) Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. Integr Comp Biol. doi:10.1093/icb/ict004

    PubMed  Google Scholar 

  42. Springer P, Boggs CL (1986) Resource Allocation to oocytes: heritable variation with altitude in Colias philodice eriphyle (Lepidoptera). Am Nat 127:252–256. http://www.jstor.org/stable/2461354

  43. Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830. doi:10.1098/rspb.2010.1295

    Article  PubMed  PubMed Central  Google Scholar 

  44. Sunday JM et al (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci 111:5610–5615. doi:10.1073/pnas.1316145111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Watt WB (1968) Adaptive significance of pigment polymorphisms in Colias butterflies. I. Variation of melanin pigment in relation to thermoregulation. Evolution 22:437–458. doi:10.2307/2406873

    Article  Google Scholar 

  46. Watt WC, France, Snyder L, Watt A, Rothschild D (1977) Population structure of pierid butterflies. Oecologia 27:1–22. doi:10.1007/bf00345682

    Article  Google Scholar 

  47. Williams JW, Jackson ST, Kutzbacht JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. Proc Natl Acad Sci USA 104:5738–5742. doi:10.1073/pnas.0606292104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Woods AH, Bonnecaze RT (2006) Insect eggs at a transition between diffusion and reaction limitation: temperature, oxygen, and water. J Theor Biol 243:483–492. doi:10.1016/j.jtbi.2006.07.008

    Article  Google Scholar 

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Acknowledgments

We thank the City of Gunnison, the City of Montrose, and Robert and Roxanne Lane of Dayspring Farms for access to collection sites. We also thank the Rocky Mountain Biological Laboratory for access to lab space. We thank Kati Moore for her tireless work with the egg thermal gradient and Edward Shin for the countless hours scoring egg-hatching videos. We thank Kate Augustine, Samuel Shuford, and Autumn Arciero for help with field experiments. We also thank the reviewers and Rob Dunn for useful edits on the manuscript. The research was supported in part by NSF Grants DEB-1120062 to L. B. B. and J. G. K. and IOS-1120500 to J. G. K.

Author contribution statement

H. J. M., L. B. B., and J. G. K. conceived and designed the experiments. H. J. M. and J. K. H. performed the experiments. H. J. M. and J. G. K. analyzed the data. H. J. M. and J. G. K. wrote the manuscript; other authors provided editorial advice.

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Correspondence to Heidi J. MacLean.

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Communicated by Roland A. Brandl.

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MacLean, H.J., Higgins, J.K., Buckley, L.B. et al. Geographic divergence in upper thermal limits across insect life stages: does behavior matter?. Oecologia 181, 107–114 (2016). https://doi.org/10.1007/s00442-016-3561-1

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Keywords

  • Colias
  • Wing melanin
  • Overheating
  • Heat shock
  • Thermoregulation