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Seasonal phenotypic plasticity: wild ladybirds are darker at cold temperatures

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Abstract

Seasons vary in the average environmental conditions a species experiences, meaning that optimum strategies for concealment or feeding may also vary. Populations of the ladybird Harmonia axyridis contain both melanic and non-melanic forms and changes in allele frequency in some populations suggest that melanism may be advantageous in winter, but costly in summer. This could favour the evolution of phenotypic plasticity in colour pattern, as individuals which changed colour throughout the year would be able to maximise their fitness. We have previously shown in the laboratory that melanisation in the “non-melanic” morph of H. axyridis, f. succinea, is predominantly controlled by temperature during development. We now report that wild populations of H. axyridis f. succinea also conform to this principle: lower field temperatures during development produce individuals with more and larger spots. Furthermore, we have found that the critical period of development where temperature affects the level of melanisation covers the pupal and late larval stages, and melanisation increases with the length of time spent at cold temperature. We conclude it is likely that the temperature experienced during this period is used to predict the temperature encountered as an adult. This may allow individuals to produce the level of melanisation necessary to maintain activity levels at the temperatures encountered when they emerge. The long sensitive period seen in H. axyridis may be in order to avoid mismatches between melanisation and seasonal environment.

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References

  • Alpert P, Simms EL (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust?. Evol Ecol 16(3):285–297

    Article  Google Scholar 

  • Banta JA, Dole J, Cruzan MB, Pigliucci M (2007) Evidence of local adaptation to coarse-grained environmental variation in Arabidopsis thaliana. Evolution 61(10):2419–2432. doi:10.1111/j.1558-5646.2007.00189.x

    Article  PubMed  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Annual Rev Ecol Evol Syst 38:1–25. doi:10.1146/annurev.ecolsys.37.091305.110115

    Article  Google Scholar 

  • Brakefield PM, French V (1999) Butterfly wings: the evolution of development of colour patterns. Bioessays 21(5):391–401

    Article  Google Scholar 

  • Brakefield PM, Reitsma N (1991) Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol Entomol 16(3):291–303

    Article  Google Scholar 

  • Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384(6606):236–242

    Article  PubMed  CAS  Google Scholar 

  • Dobzhansky T (1924) Die geographische und individuelle Variabilität von Harmonia axyridis Pall. in ihren Wechselbeziehungen. Biologische Zentralblatt 44:401–421

    Google Scholar 

  • Dobzhansky T (1933) Geographical variation in lady-beetles. Am Nat 67:97–126

    Article  Google Scholar 

  • Gomulkiewicz R, Kirkpatrick M (1992) Quantitative genetics and the evolution of reaction norms. Evolution 46(2):390–411

    Article  Google Scholar 

  • Grill CP (1999) Development of colour in an aposematic ladybird beetle: The role of environmental conditions. Evol Ecol Res 1(6):651–662

    Google Scholar 

  • Hendry AP, Kinnison MT (2001) An introduction to microevolution: rate, pattern, process. Genetica 112:1–8

    Article  PubMed  Google Scholar 

  • Hosino Y (1940) Genetical studies on the pattern types the lady-bird beetle, Harmonia axyridis Pallas. J Genet 40(1/2):215–228

    Article  Google Scholar 

  • Jiang W, Pan X, Liu J, Liu L (2008) Studies on the type of spot on the wing of Harmonia axyridis (Pallas) in Baoding. Hebei J Forest Orch Res 22:198–202

    Google Scholar 

  • Jing Y, Zhang Y (2001) Studies on the type of spot on the wing of Harmonia axyridis (Pallas) in Shanxi Province. J Shanxi Agric Univ 4:42–45

    Google Scholar 

  • Komai T (1956) Genetics of ladybeetles. Adv Genet Incorp Mole Genet Med 8:155–188

    Google Scholar 

  • Kooi RE, Brakefield PM (1999) The critical period for wing pattern induction in the polyphenic tropical butterfly Bicyclus anynana (Satyrinae). J Insect Physiol 45(3):201–212

    Article  PubMed  CAS  Google Scholar 

  • Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton

    Google Scholar 

  • Michie LJ, Mallard F, Majerus M, Jiggins F (2010) Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J Evol Biol 23(8):1699–1707

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer, Berlin

    Book  Google Scholar 

  • Reed TE, Waples RS, Schindler DE, Hard JJ, Kinnison MT (2010) Phenotypic plasticity and population viability: the importance of environmental predictability. Proc Royal Soc Lond Ser B Biol Sci 277(1699):3391–3400. doi:10.1098/rspb.2010.0771

    Article  Google Scholar 

  • Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112:183–198

    Article  PubMed  Google Scholar 

  • Rountree DB, Nijhout HF (1995) Hormonal control of a seasonal polyphenism in Precis coenia (Lepidoptera, Nymphalidae). J Insect Physiol 41(11):987–992

    Article  CAS  Google Scholar 

  • Salamin N, Wuest RO, Lavergne S, Thuiller W, Pearman PB (2010) Assessing rapid evolution in a changing environment. Trend Ecol Evol 25(12):692–8

    Article  Google Scholar 

  • Shapiro AM (1976) Seasonal polyphenism. Evol Biol 9:259–333

    Google Scholar 

  • Tan CC (1946) Mosaic dominance in the inheritance of color patterns in the lady-bird beetle, Harmonia axyridis. Genetics 31(2):195–210

    Google Scholar 

  • Tan CC, Li JC (1934) Inheritance of the elytral color patterns of the lady-bird beetle, Harmonia axyridis Pallas. Am Natur 68:252–265

    Article  Google Scholar 

  • Trullas SC, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32(5):235–245

    Article  Google Scholar 

  • Via S, Gomulkiewicz R, deJong G, Scheiner SM, Schlichting CD, Vantienderen PH (1995) Adaptive phenotypic plasticity—consensus and controversy. Trend Ecol Evol 10(5):212–217

    Article  CAS  Google Scholar 

  • Yuan R, Zhang F, Wen G (1994) Color pattern of Harmonia axyridis in Changbai Mountains. Jilin Agric Sci 4:45–54

    Google Scholar 

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Acknowledgements

We thank Emma Rhule and Ian Wright for assistance with practical work. FMJ is funded by a Royal Society University Research Fellowship.

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Correspondence to Laura Jane Michie.

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Michie, L.J., Masson, A., Ware, R.L. et al. Seasonal phenotypic plasticity: wild ladybirds are darker at cold temperatures. Evol Ecol 25, 1259–1268 (2011). https://doi.org/10.1007/s10682-011-9476-8

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