Skip to main content
Log in

Genetic architecture and phenotypic plasticity of thermally-regulated traits in an eruptive species, Dendroctonus ponderosae

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Phenotypic plasticity in thermally-regulated traits enables close tracking of changing environmental conditions, and can thereby enhance the potential for rapid population increase, a hallmark of outbreak insect species. In a changing climate, exposure to conditions that exceed the capacity of existing phenotypic plasticity may occur. Combining information on genetic architecture and trait plasticity among populations that are distributed along a latitudinal cline can provide insight into how thermally-regulated traits evolve in divergent environments and the potential for adaptation. Dendroctonus ponderosae feed on Pinus species in diverse climatic regimes throughout western North America, and show eruptive population dynamics. We describe geographical patterns of plasticity in D. ponderosae development time and adult size by examining reaction norms of populations from multiple latitudes. The relative influence of additive and non-additive genetic effects on population differences in the two phenotypic traits at a single temperature is quantified using line-cross experiments and joint-scaling tests. We found significant genetic and phenotypic variation among D. ponderosae populations. Simple additive genetic variance was not the primary source of the observed variation, and dominance and epistasis contributed greatly to the genetic divergence of the two thermally-regulated traits. Hybrid breakdown was also observed in F2 hybrid crosses between northern and southern populations, further indication of substantial genetic differences among clinal populations and potential reproductive isolation within D. ponderosae. Although it is unclear what maintains variation in the life-history traits, observed plasticity in thermally-regulated traits that are directly linked to rapid numerical change may contribute to the outbreak nature of D. ponderosae, particularly in a changing climate.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amman GD, Cole WE (1983) Mountain pine beetle dynamics in lodgeple pine forests. Part II. Population dynamics. USDA Forest Service, Gen. Tech. Rep. INT-145, Ogden, UT

  • Amman GD, Pace VE (1976) Optimum egg gallery densities for the mountain pine beetle in relation to lodgepole pine phloem thickness. USDA Forest Service, Res. Note INT-209, Ogden, UT

  • Atkinson D (1994) Temperature and organisms size–a biological law for ectotherms? Adv Ecol Res 3:1–58

    Article  Google Scholar 

  • Barbosa P, Baltensweiler W (1987) Phenotypic plasticity and herbivore outbreaks. In: Barbosa P, Schultz J (eds) Insect outbreaks. Academic Press, New York, pp 469–504

    Google Scholar 

  • Bentz BJ, Mullins DE (1999) Ecology of mountain pine beetle cold hardening in the Intermountain West. Environ Entomol 28(4):577–587

    Google Scholar 

  • Bentz BJ, Logan JA, Amman GD (1991) Temperature dependent development of the mountain pine beetle (Coleoptera: Scolytidae), and simulation of its phenology. Can Entomol 123:1083–1094

    Article  Google Scholar 

  • Bentz BJ, Logan JA, Vandygriff JC (2001) Latitudinal life history variation in Dendroctonus ponderosae (Coleoptera: Scolytidae) development time and size. Can Entomol 133:375–387

    Article  Google Scholar 

  • Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hicke J, Hayes JL, Kelsey R, Negrón J et al (2010) Climate change and bark beetles of the western US and Canada: direct and indirect effects. Bioscience 60:602–613

    Article  Google Scholar 

  • Blows MW, Sokolowski MB (1995) The expression of additive and nonadditive genetic variation under stress. Genetics 140:1149–1159

    PubMed  CAS  Google Scholar 

  • Bracewell RA, Pfrender ME, Mock KE, Bentz BJ (2010) Cryptic postzygotic isolation in an eruptive species of bark beetle (Dendroctonus ponderosae). Evolution. doi:10.1111/j.1558-5646.2010.01201.x

  • Bradshaw WE, Holzapfel CM (2000) The evolution of genetic architectures and the divergence of natural populations. In: Wolf JB, Brodie ED III, Wade MJ (eds) Epistasis and the evolutionary process. Oxford University Press, New York, pp 245–263

    Google Scholar 

  • Bradshaw WE, Holzapfel CM (2008) Genetic response to rapid climate change: it’s seasonal timing that matters. Mol Ecol 17:157–166

    Article  PubMed  CAS  Google Scholar 

  • Calabrese JM, Fagan WF (2004) Lost in time, lonely and single: reproductive asynchrony and the Allee effect. Am Nat 164:25–37

    Article  PubMed  Google Scholar 

  • Danilevskii AS (1965) Photoperiodism and seasonal development of insects. Oliver and Boyd, London

    Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  PubMed  CAS  Google Scholar 

  • Elkin CM, Reid ML (2005) Low energy reserves and energy allocation decisions affect reproduction by mountain pine beetles (Dendroctonus ponderosae). Funct Ecol 19:102–109

    Article  Google Scholar 

  • Ellers J, Driessen G (2010) Genetic correlations between temperature-induced plasticity of life-history traits in a soil arthropod. Evol Ecol. doi:10.1007/s10682-010-9414-1

  • Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Ann Rev Ecol Syst 28:659–687

    Article  Google Scholar 

  • Fox CW, Stillwell RC, Amarillo-S AR, Czesal ME, Messina FJ (2004) Genetic architecture of population differences in oviposition behavior of the seed beetle Callosobruchus maculates. J Evol Biol 17:1141–1151

    Article  PubMed  CAS  Google Scholar 

  • Gibert P, Capy P, Imasheva A, Moreteau B, Morin JP, Petavy G et al (2004) Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120:165–179

    Article  PubMed  CAS  Google Scholar 

  • Gibson K, Skov K, Kegley S, Jorgensen C, Smith S, Witcosky J (2008) Mountain pine beetle impacts in high-elevation five-needle pines: current trends and challenges, R1-08-020, US Department of Agriculture, Forest Service, Northern Region, Missoula, Montana

  • Gilchrist AS, Partridge L (1999) A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153:1775–1787

    PubMed  CAS  Google Scholar 

  • Godbout J, Fazekas A, Newton CH, Yeh FC, Bousquet J (2008) Glacial vicariance in the Pacific Northwest: evidence from a lodgepole pine mitochondrial DNA minisatellite for multiple genetically distinct and widely separated refugia. Mol Ecol 17:2463–2475

    Article  PubMed  CAS  Google Scholar 

  • Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3–17

    Article  Google Scholar 

  • Holloway GJ, DE Jong PW, Ottenheim M (1993) The genetics and cost of chemical defense in the two-spot ladybird (Adalia bipunctata L.). Evolution 47(4):1229–1239

    Article  Google Scholar 

  • Honek A (1993) Intraspecific variation in body size and fecundity in insects. Oikos 66:483–492

    Article  Google Scholar 

  • Hunter AF, Elkinton JS (2000) Effects of synchrony with host plant populations of a spring-feeding Lepidopteran. Ecology 81:1248–1261

    Article  Google Scholar 

  • IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of working group I to the fourth assessment. Report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 996

    Google Scholar 

  • Keller LK, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268

    Google Scholar 

  • Kozol AJ, Scott MP, Traniello JFA (1988) The American burying beetle: studies on the natural history of a declining species. Psyche 95:167–176

    Article  Google Scholar 

  • Lair KP, Bradshaw WE, Holzapfel CM (1997) Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 147:1873–1883

    PubMed  CAS  Google Scholar 

  • Lardies MA, Bozinovic F (2008) Genetic variation for plasticity in physiological and life-history traits among populations of an invasive species, the terrestrial isopod Porcellio laevis. Evol Ecol Res 10:747–762

    Google Scholar 

  • Latta LC, Bakelar JW, Knapp RA, Pfrender ME (2007) Rapid evolution in response to introduced predators II: the contribution of adaptive plasticity. BMC Evol Biol 7:21

    Article  PubMed  Google Scholar 

  • Logan JA, Bentz BJ (1999) Model analysis of mountain pine beetle (Coleoptera: Scolytidae) seasonality. Environ Entomol 28:924–934

    Google Scholar 

  • Logan JA, Bentz BJ, Vandygriff JC, Turner DL (1998) General program for determining instar distributions from headcapsule widths: example analysis of mountain pine beetle data. Environ Entomol 27(3):555–563

    Google Scholar 

  • Lyon RL (1958) A useful secondary sex character in Dendroctonus bark beetles. Can Entomol 90:582–584

    Article  Google Scholar 

  • Mather K, Jinks JL (1982) Biometrical genetics: the study of continous variation, 3rd edn. Chapman and Hall, New York

    Google Scholar 

  • Mock KE, Bentz BJ, O’Neill EM, Chong JP, Orwin J, Pfrender ME (2007) Landscape-scale genetic variation in a forest outbreak species, the mountain pine beetle (Dendroctonus ponderosae). Mol Ecol 16:553–568

    Article  PubMed  CAS  Google Scholar 

  • Nijhout FH, Roff DA, Davidowitz G (2010) Conflicting processes in the evolution of body size and development time. Philos Trans R Soc B 365:567–575

    Article  Google Scholar 

  • Nylin S, Wickman PO, Wiklund C (1989) Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae). Biol J Linn Soc 38:155–171

    Article  Google Scholar 

  • Ott L (1977) An introduction to statistical methods and data analysis. Duxbury Press, Massachusetts

    Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692

    Article  PubMed  Google Scholar 

  • Powell JA, Bentz BJ (2009) Connecting phenological predictions with population growth rates for mountain pine beetle, an outbreak insect. Landscape Ecol 24:657–672

    Article  Google Scholar 

  • Powell J, Jenkins J, Logan J, Bentz BJ (2000) Seasonal temperature alone can synchronize life cycles. Bull Math Biol 62:977–998

    Article  PubMed  CAS  Google Scholar 

  • Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: dynamics of biome-wide bark beetle eruptions. Bioscience 58:501–518

    Article  Google Scholar 

  • Régnière J, Bentz B (2007) Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. J Insect Physiol 53:559–572

    Article  PubMed  Google Scholar 

  • Régnière J, St-Amant R (2007) Stochastic simulation of daily air temperature and precipitation from monthly normals in North America north of Mexico. Int J Biometeorol 51:415–430

    Article  PubMed  Google Scholar 

  • Reid RW (1962) Biology of the mountain pine beetle, Dendroctonus monticolae, in the east Kootenay region of British Columbia I. life cycle, brood development, and flight periods. Can Entomol 94:531–538

    Article  Google Scholar 

  • Reid ML, Baruch O (2010) Mutual mate choice by mountain pine beetles: size-dependence but not size-assortative mating. Ecol Entomol 35:69–76

    Article  Google Scholar 

  • Richardson BA, Brunsfeld SJ, Klopfenstein NB (2002) DNA from bird-dispersed seed and wind-disseminated pollen provides insights into postglacial colonization and population genetic structure of whitebark pine (Pinus albicaulis). Mol Ecol 11:215–227

    Article  PubMed  CAS  Google Scholar 

  • Roff DA (1992) The evolution of life histories. Chapman and Hall, New York

    Google Scholar 

  • Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60:1981–1990

    PubMed  Google Scholar 

  • Safranyik L, Whitney HS (1985) Development and survival of axenically reared mountain pine beetles, Dendroctonus ponderosae, at constant temperatures. Can Entomol 117:185–192

    Article  Google Scholar 

  • Safranyik L, Carroll AL, Regniere J, Langor DW, Riel WG, Shore TL et al (2010) Potential for range expansion of mountain pine beetle into the boreal forest of North America. Can Entomol 142:415–442

    Article  Google Scholar 

  • Schiffer M, Gilchrist AS, Hoffmann AA (2006) The contrasting genetic architecture of wing size, viability, and development time in a rainforest species and its more widely distributed relative. Evolution 60:106–114

    PubMed  Google Scholar 

  • Scoville AG, Pfrender ME (2010) Phenoptypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc Nat Acad Sci USA 107:4260–4263

    Article  PubMed  CAS  Google Scholar 

  • Sgro CM, Blows MW (2003) Evolution of additive and nonadditive genetic variance in development time along a cline in Drospholia serrata. Evolution 57:1846–1851

    PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Sturgeon KB, Mitton JB (1986) Allozyme and morphological differentiation of mountain pine beetles, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), associated with host tree. Evolution 40:290–302

    Article  Google Scholar 

  • Taylor F (1981) Ecology and evolution of physiological time in insects. Am Nat 117:1–23

    Article  Google Scholar 

  • van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Ann Rev Entomol 52:37–55

    Article  Google Scholar 

  • Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522

    Article  Google Scholar 

  • Whitlock MC, Phillips PC, Moore FB, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Syst 26:601–629

    Article  Google Scholar 

Download references

Acknowledgments

Jim Vandygriff and Matt Hansen provided invaluable assistance with collection of D. ponderosae-infested trees and laboratory rearing of beetles. We thank Alan Dymerski for collection of the South Dakota population, and Laura Merrill for help locating the California populations. The USDA Forest Service, Rocky Mountain Research Station and Forest Health Monitoring contributed funding for this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara J. Bentz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bentz, B.J., Bracewell, R.R., Mock, K.E. et al. Genetic architecture and phenotypic plasticity of thermally-regulated traits in an eruptive species, Dendroctonus ponderosae . Evol Ecol 25, 1269–1288 (2011). https://doi.org/10.1007/s10682-011-9474-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9474-x

Keywords

Navigation