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Environmentally-based maternal effects: a hidden force in insect population dynamics?

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Summary

The nutritional environment of the parental generation of the polyphagous gypsy moth, Lymantria dispar, can significantly influence the growth and reproductive potential of the next generation through environmentally-based maternal effects. In the first experiment, members of the parental generation were reared on red oak trees (Quercus rubra L.) with known defoliation and phenolic levels. Diet in the offspring generation was homogeneous (synthetic diet). With genetic effects accounted for 1) offspring attained greater pupal weights when their mothers fed on trees with higher leaf damage levels, 2) daughters had a shorter prefeeding stage, a trait associated with dispersal tendency, when their mothers experienced higher condensed tannin levels, and 3) sons had lower pupal weights when their mothers experienced greater condensed tannin levels. In the second experiment, members of the parental generation were reared on either red or black oak (Q. velutina) trees. Offspring of each mother were divided among four diets: red oak, chestnut oak (Q. prinus L.), a standard synthetic diet, and a low-protein synthetic diet. The parental host species accounted for 24% of the variation in daughters' development time; offspring diet accounted for 52%. When mothers were reared on black oak rather than red oak, their offspring developed significantly faster when the F1 diet was chestnut oak. Environmentally-based maternal effects can significantly influence the expression of offspring dispersal potential, growth rate, and offspring fecundity. These traits contribute to natality and survival in natural populations and, hence, to population growth potential. Theoretical models of insect population dynamics demonstrate that the presence of a time delay in a density dependent response can induce destabilization. Maternal effects act on a time delay and may participate in the destabilization characteristic of outbreak species.

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References

  • Andrewartha HG, Birch LC (1954) The distribution and abundance of animals. University of Chicago Press, Chicago, Ill, USA

    Google Scholar 

  • Atchley WR, Newman S (1989) A quantitative genetic perspective on mammalian development. Am Nat 134: 486–512

    Google Scholar 

  • Berryman AA (1978) Towards a theory of insect epidemiology. Res Popul Ecol 19:181–196

    Google Scholar 

  • Berryman AA (1981) Population Systems: A General Introduction. Plenum Press, NY

    Google Scholar 

  • Berryman AA (1987) The theory and classification of outbreaks. In: Barbosa P, Schultz JC (eds.) Insect Outbreaks Academic Press, New York pp. 3–30

    Google Scholar 

  • Cain ML, Eccleston J, Kareiva PM (1985) The influence of food plant dispersion on caterpillar searching success. Ecol Entomol 10:1–7

    Google Scholar 

  • Campbell IM (1962) Reproductive capacity in the genus Choristoneura Led. (Lepidoptera: Tortricidae). I. Quantitative inheritance and genes as controllers of rates. Can J Genet Cytol 4:272–288

    Google Scholar 

  • Capinera JL, Barbosa P (1976) Dispersal of first-instar gypsy moth larvae in relation to population quality. Oecologia 26:53–60

    Google Scholar 

  • Caswell H (1972) A simulation study of a time lag population model. J Theor Biol 34:419–439

    Google Scholar 

  • Cheng L (1970) Timing the attack by Lyphia dubia Fall. (Diptera: Tachinidae) on the winter moth Operophtera brumata (L.) (Lepidoptera: Geometridae) as a factor affecting parasite success. J Animal Ecol 39:313–320

    Google Scholar 

  • Falconer DS, (1965) Maternal effects and selection response. In: Geerts SJ (ed.) Genetics Today, Proceedings of the XI International Congress on Genetics vol. 3, pp. 763–774. Pergamon, Oxford

    Google Scholar 

  • Feeny P (1970) Seasonal changes in oak lea tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581

    Google Scholar 

  • Giese RL, Schneider ML (1979) Cartographic comparisons of Eurasian gypsy moth distribution. Entomol News 90:1–16

    Google Scholar 

  • Gould F (1988) Stress specificity of maternal effects in Heliothis virescens (Boddie) (Lepidoptera: Noctuidae) larvae. Mem Entomol Soc Can 146:191–197

    Google Scholar 

  • Gould JR, Elkinton JS, Wallner WE (1990) Density dependent suppression of experimetnally created gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae) populations by natural enemies. J Ani Ecol 59:213–233

    Google Scholar 

  • Harvey GT (1977) Mean weight and rearing performance of successive egg clusters of eastern spruce budworm (Lepidoptera: Tortricidae). Can Entomol 109:487–496

    Google Scholar 

  • Haukioja E, Neuvonen S (1985) The relationship between size and reproductive potential in male and female Epirrita autumnata (Lepidoptera: Geometridae). Ecol Entomol 10:417–427

    Google Scholar 

  • Haukioja E, Neuvonen S (1987) Insect population dynamics and induction of plant resistance: The testing of hypotheses. In: Barbosa P, Schultz JC (eds.) Insect Outbreaks Academic Press, New York, pp. 411–432

    Google Scholar 

  • Hunter MD (1990) Differential susceptibility to variable plant phenology and its role in competition between two insect herbivores on oak. Ecol Entomol 15:401–408

    Google Scholar 

  • Janssen GM, De Jong G, Joose ENG, Scharloo W (1988) A negative maternal effect in springtails. Evolution 42:828–834

    Google Scholar 

  • Kirkpatrick M, Lande R (1989) The evolution of maternal effects. Evolution 43:485–503

    Google Scholar 

  • Leonard DE (1968) Sexual differentiation in time of hatch of eggs of the gypsy moth. J Econ Entomol 61:698–700

    Google Scholar 

  • Leonard DE (1970) Intrinsic factors causing qualitative changes in populations of Porthetria dispar (Lepidoptera: Lymantriidae). Can Entomol 102:239–249

    Google Scholar 

  • Leonard DE (1971) Air-borne dispersal of the gypsy moth and its influence on concepts of control. J Econ Entomol 64:638–641

    Google Scholar 

  • Magnoler A (1974) Bioassay of a nuclear polyhedrosis virus of the gypsy moth, Porthetria dispar. J Invertab Pathol 23:190–196

    Google Scholar 

  • May RM Conway GR, Hassell MP, Southwood TRE (1974) Time-delays, density-dependence and single-species oscillations. J Anim Ecol 43:747–770

    Google Scholar 

  • McManus ML (1973) The role of behavior in the dispersal of newly hatched gypsy moth larvae. USDA-FS Research Paper NE-267

  • Moran N, Hamilton WD (1980) Low nutritive quality as defense against herbivores. J Theor Biol 86:247–254

    Google Scholar 

  • Morris RF (1967) Influence of parental food quality on the survival of Hyphantria cunea. Can Entomol 99:24–33

    Google Scholar 

  • Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annu. Rev Entomol 36:511–534

    Google Scholar 

  • Neter JW, Wasserman W, Kutner MH (1985) Applied Linear Statistical Moldels. Richard D. Irwin, Inc. Homewood, IL

    Google Scholar 

  • ODell TM, Rollinson W (1966) A technique for rearing the gypsy moth on an artificial diet. J Econ Entomol 59:741–742

    Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three tropic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Systems 11:41–65

    Google Scholar 

  • Ramachandran R (1987) Influence of host plants on the wind dispersal and the survival of an Australian geometrid caterpillar. Entom Experiment Applic 44:289–294

    Google Scholar 

  • Riska B, Rutledge JJ, Atchley WR (1985) Covariance between direct and maternal effects in mice, with a model of persistant environmental influences. Gen Res 45:287–297

    Google Scholar 

  • Roach DA, Wulff RD (1987) Maternal effects in plants. Ann Rev Ecol Syst 18:209–235

    Google Scholar 

  • Rossiter MC (1987a) Genetic and phenotypic variation in diet breadth in a generalist herbivore. Evol Ecol 1:272–282

    Google Scholar 

  • Rossiter MC (1987b) Use of secondary hosts by non-outbreak populations of the gypsy moth. Ecology 68:857–868

    Google Scholar 

  • Rossiter MC, Schultz JC, Baldwin IT (1988) Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277

    Google Scholar 

  • Rossiter MC, Yendol WG, Dubois NR (1990) Resistance to Bacillus thuringiensis in gypsy moth (Lepidoptera: Lymantriidae): Genetic and environmental causes. J Econ Entomol 83(6):2211–2218

    Google Scholar 

  • Rossiter MC (1991a) The impact of resource variation on population quality in herbivorous insects: A critical component of population dynamics. In: Hunter MD, Ohgushi T, Price PW (eds.) Resource distribution and animal-plant interactions, Chapter 2, Academic Press, San Diego (in press)

    Google Scholar 

  • Rossiter MC (1991b) Maternal effects generate variation in life history: consequences of egg weight plasticity in the gypsy moth. Funct Ecol 5(3):

  • SAS Institute, Inc. (1985) SAS User's Guide: Statistics. Cary, NC

  • Schroeder LA (1986) Changes in tree leaf quality and growth performance of lepidopteran larvae. Ecology 67:1628–1636

    Google Scholar 

  • Schultz JC, Nothnagle PJ, Baldwin IT (1982) Seasonal and individual variation in leaf quality of two northern hardwood species. Am J Bot 69:753–759

    Google Scholar 

  • Slansky F, Scriber JM (1985) Food consumption and utilization. In Kerku GA, Gilbert LI (eds.) “Comprehensive Insect Physiology, Biochemistry, and Pharmacology” vol 4, Pergamon, Oxford pp. 87–163

    Google Scholar 

  • Wellington WG (1957) Individual differences as a factor in population dynamics: The development of a problem. Can J Zool 35:293–323

    Google Scholar 

Download references

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Rossiter, M.C. Environmentally-based maternal effects: a hidden force in insect population dynamics?. Oecologia 87, 288–294 (1991). https://doi.org/10.1007/BF00325268

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