Hostname: page-component-7f64f4797f-n5rmq Total loading time: 0 Render date: 2025-11-04T11:18:47.191Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal effects shape dynamic trajectories of reproductive allocation in the ladybird Coleomegilla maculata

Published online by Cambridge University Press:  05 April 2012

G. Vargas ,
J.P. Michaud  and
J.R. Nechols
G. Vargas
Affiliation:
Agricultural Research Center-Hays, Kansas State University, 1232 240th Avenue, Hays, KS, 67601, USA Department of Entomology, Kansas State University, Manhattan, KS, 66506, USA
J.P. Michaud*
Affiliation:
Agricultural Research Center-Hays, Kansas State University, 1232 240th Avenue, Hays, KS, 67601, USA
J.R. Nechols
Affiliation:
Department of Entomology, Kansas State University, Manhattan, KS, 66506, USA
*
*Author for correspondence Fax: 785-623-4369 E-mail: jpmi@ksu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

We followed lifetime trajectories of reproductive allocation in Coleomegilla maculata females of three different size classes produced by rearing beetles on three different daily larval feeding regimes (30 min, 6 h or ad libitum access to eggs of Ephestia kuehniella). We hypothesized that small females would produce fewer and smaller eggs than larger females and that reproductive effort would decline with female age. Females were mated with a male from the same treatment and then isolated with ad libitum food for their entire adult lives. Egg size increased over time in all treatments; small females started off laying the smallest eggs, but increased egg size more rapidly than larger females, until all treatments converged on a similar egg size around the 20th day of oviposition. Large females realized a larger proportion of their fecundity early in life, but smaller females increased daily fecundity over time. Reproductive effort (egg mass/body mass) did not decline over 30 oviposition days; it remained constant in large females, but increased among small and medium females, suggesting gradual compensation for larval food deprivation. An increase in egg size with maternal age may be an adaptive strategy to maximize fitness on ephemeral patches of aphid prey, assuming females reproduce in a single aphid outbreak and that offspring produced later in the aphid cycle experience greater competition and risk of mortality compared to those produced earlier. We demonstrate for the first time in Coleoptera that dynamic changes in both egg size and number occur as a function of female age and illustrate that such changes are constrained by larval feeding histories via their effects on maternal body size.

Keywords

aphidophagybody sizeegg sizefecundityreproductive effort

Information

Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 5 , October 2012 , pp. 558 - 565
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Benton, T.G., Plaistow, S.J., Beckerman, A.P., Lapsley, C.T. & Littlejohns, S. (2005) Changes in maternal investment in eggs can affect population dynamics. Proceedings of the Royal Society of London, Series B 272, 1351–1356.Google Scholar
Benton, T.G., St. Clair, J.J.H. & Plaistow, S.J. (2008) Maternal effects mediated by maternal age: from life histories to population dynamics. Journal of Animal Ecology 77, 1038–1046.Google Scholar
Bernardo, J. (1996) The particular maternal effect of propagule size, especially egg size: Patterns, models, quality of evidence and interpretations. American Zoologist 36, 216–236.CrossRefGoogle Scholar
Brockelman, W.Y. (1975) Competition, the fitness of offspring, and optimal clutch size. American Naturalist 109, 677–699.Google Scholar
Crump, M.L. (1981) Variation in propagule size as a function of environmental uncertainty for tree frogs. American Naturalist 117, 724–737.CrossRefGoogle Scholar
da Silva, R.B., Cruz, I., Figueiredo, M. de L.C. & Tavares, W. de S. (2010) Development of Coleomegilla maculata De Geer (Coleoptera: Coccinellidae) with prey and artificial diet. Revista Brasileira de Milho e Sorgo 9, 13–26.CrossRefGoogle Scholar
Dixon, A.F.G. (1958) The escape response shown by certain aphids to the presence of the coccinellid Adalia decimpunctata (L.) Transactions of the Royal Entomological Society of London 110, 319–334.CrossRefGoogle Scholar
Dixon, A.F.G. (2000) Insect Predator-Prey Dynamics. Cambridge, UK, Cambridge University Press.Google Scholar
Dixon, A.F.G. & Agarwala, B.K. (2002) Triangular fecundity function and ageing in ladybird beetles. Ecological Entomology 27, 433–440.CrossRefGoogle Scholar
Dixon, A.F.G & Guo, Y. (1993) Egg and cluster size in ladybird beetles (Coleoptera: Coccinellidae): the direct and indirect effects of aphid abundance. European Journal of Entomology 90, 457–463.Google Scholar
Einum, S. & Fleming, I.A. (2000) Maternal effects of egg size in brown trout (Salmo truta): norms of reaction to environmental quality. Proceedings of the Royal Society of London, Series B 266, 2095–2100.CrossRefGoogle Scholar
Fischer, K., Bot, A.N.M., Zwaan, B.J. & Brakefield, P.M. (2004) Genetic and environmental sources of egg size variation in the butterfly Bicyclus anynana. Heredity 92, 163–169.CrossRefGoogle ScholarPubMed
Fischer, B., Taborsky, B. & Kokko, H. (2011) How to balance the offspring quality–quantity tradeoff when environmental cues are unreliable. Oikos 120, 258–270.CrossRefGoogle Scholar
Fox, C.W. & Czesak, M.E. (2000) Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45, 341–369.CrossRefGoogle ScholarPubMed
Fox, C.W. & Mousseau, T.H. (1998) Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. pp. 159–177in Mousseau, T. & Fox, C. (Eds) Maternal Effects as Adaptations. Oxford, UK, Oxford University Press.Google Scholar
Heath, D.D., Heath, J.W., Bryden, C.A., Johnson, R.M. & Fox, C.W. (2003) Rapid evolution of egg size in captive salmon. Science 299, 1738.CrossRefGoogle ScholarPubMed
Heisswolf, A., Klemola, T., Andersson, T. & Ruohomaki, K. (2009) Shifting body weight-fecundity relationship in a capital breeder: maternal effects on egg numbers of the autumnal moth under field conditions. Bulletin of Entomological Research 99, 73–81.CrossRefGoogle Scholar
Hodek, I. (1996) Food Relationships. pp. 143–238in Hodek, I. & Honek, A. (Eds) Ecology of Coccinellidae. Dordrecht, Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Honěk, A. (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66, 483–492.Google Scholar
Honěk, A., Dixon, A.F.G. & Martinkov, Z. (2008a) Body size and the temporal sequence in the reproductive activity of two species of aphidophagous coccinellids exploiting the same resource. European Journal of Entomology 105, 421–425.CrossRefGoogle Scholar
Honěk, A., Dixon, A.F.G. & Martinkov, Z. (2008b) Body size, reproductive allocation, and maximum reproductive rate of two species of aphidophagous Coccinellidae exploiting the same resource. Entomologia Experimentalis et Applicata 127, 1–9.CrossRefGoogle Scholar
Hutchings, J.A. (1991) Fitness consequences of variation in egg size and food abundance in brook trout Salvelinus fontinalis. Evolution 45, 1162–1168.CrossRefGoogle ScholarPubMed
Kajita, Y. & Evans, E.W. (2009) Ovarian dynamics and oosorption in two species of predatory lady beetles (Coleoptera: Coccinellidae). Physiological Entomology 34, 185–194.CrossRefGoogle Scholar
Kajita, Y. & Evans, E.W. (2010) Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Annals of the Entomological Society of America 103, 750–756.Google Scholar
Kaplan, R.H. & Cooper, W.S. (1984) The evolution of developmental plasticity in reproductive characteristics: an application of the ‘adaptive coin-flipping’ principle. –American Naturalist 123, 393–410.CrossRefGoogle Scholar
Kindlmann, P. & Dixon, A.F.G. (1993) Optimal foraging in ladybird beetles (Coleoptera: Coccinelidae) and its consequences in their use in biological control. Europeam Journal of Entomology 90, 443–450.Google Scholar
Kindlmann, P. & Dixon, A.F.G. (2010) Modeling population dynamics of aphids and their natural enemies. pp. 1–20in Kindlmann, P., Dixon, A.F.G. & Michaud, J.P. (Eds) Aphid Biodiversity under Environmental Change. Dordrecht, Netherlands, Springer.CrossRefGoogle Scholar
Landa, K. (1992) Adaptive seasonal variation in grasshopper offspring size. Evolution 46, 1553–1558.CrossRefGoogle ScholarPubMed
Marshall, S.D. & Gittleman, J.L. (1994) Clutch size in spiders: Is more better? Functional Ecology 8, 118–124.Google Scholar
McLain, D.K. & Mallard, S.D. (1991) Sources and adaptive consequences of egg size variation in Nezara viridula (Hemiptera: Pentatomidae). Psyche 98, 135–164.CrossRefGoogle Scholar
Michaud, J.P. (2005) On the assessment of prey suitability in aphidophagous Coccinellidae. European Journal of Entomology 102, 385–390.CrossRefGoogle Scholar
Michaud, J.P. (2012) Coccinellids in biological control. pp. 488–519in Hodek, I., van Emden, H.F. & Honěk, A. (Eds) Ecology and Behaviour of the Ladybird Beetles. West Sussex, UK, Wiley-Blackwell.Google Scholar
Michaud, J.P. & Jyoti, J.L. (2008) Dietary complementation across life stages in the polyphagous lady beetle Coleomegilla maculata. Entomologia Experimentalis et Applicata 126, 40–45.CrossRefGoogle Scholar
Michaud, J.P. & Qureshi, J.A. (2006) Reproductive diapause in Hippodamia convergens (Coleoptera: Coccinellidae) and its life history consequences. Biological Control 39, 193–200.CrossRefGoogle Scholar
Musser, F.R. & Shelton, A.M. (2003) Predation of Ostrinia nubilalis (Lepidoptera: Crambidae) eggs in sweet corn by generalist predators and the impact of alternative foods. Environmental Entomology 32, 1131–1138.Google Scholar
Ng, S.M. (1988) Observations on the foraging behaviour of starved aphidophagous coccinellid larvae (Coleoptera: Coccinellidae). pp. 29–33in Niemczyk, E. & Dixon, A.F.G. (Eds) Ecology and Effectiveness of Aphidophaga. SPB Academic Publishers.Google Scholar
Osawa, N. (2005) The effect of prey availability on ovarian development and oosorption in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology 102, 503–511.Google Scholar
Paitz, R.T., Harms, H.K., Bowden, R.M. & Janzen, F.J. (2007) Experience pays: offspring survival increases with female age. Biology Letters 3, 44–46.CrossRefGoogle ScholarPubMed
Parichy, D.M. & Kaplan, R.H. (1992) Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina orientalis. Oecologia 91, 579–586.Google Scholar
Parker, G.A. & Begon, M. (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist 128, 573–592.CrossRefGoogle Scholar
Plaistow, S.J., St. Clair, J.J.H., Grant, J. & Benton, T.G. (2007) How to put all your eggs in one basket: Empirical patterns of offspring provisioning throughout a mother's lifetime. American Naturalist 170, 520–529.Google Scholar
Räsänen, K. & Kruuk, L.E.B. (2007) Maternal effects and evolution at ecological time-scales. Functional Ecology 21, 408–421.CrossRefGoogle Scholar
Roff, D.A. (1992) The Evolution of Life Histories: Theory and Analysis. New York, USA, Chapman and Hall.Google Scholar
Santos-Cividanes, T.M., dos Anjos, A.C.R., Cividanesm, F.J. & Dias, P.C. (2011) Effects of food deprivation on the development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae). Neotropical Entomology 40, 112–116.CrossRefGoogle Scholar
SAS Institute (2008) SAS software, version 9.2. Cary, NC, USA, SAS Institute.Google Scholar
Sinervo, B. (1990) The evolution of maternal investment in lizards: an experimental and comparative analysis. Evolution 44, 279–294.Google Scholar
Sloggett, J.J. & Lorenz, M.W. (2008) Egg composition and reproductive investment in aphidophagous ladybird beetles (Coccinellidae: Coccinellini): egg development and interspecific variation. Physiological Entomology 33, 200–208.Google Scholar
Smith, C.C. & Fretwell, S.D. (1974) The optimal balance between size and number of offspring. American Naturalist 108, 499–506.Google Scholar
Specty, O., Febvay, G., Grenier, S., Delobel, B., Piotte, C., Pageaux, J.–F.Ferran, A. & Guillard, J. (2003) Nutritional plasticity of the predatory ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae): Comparison between natural and substitution prey. Archives of Insect Biochemistry and Physiology 52, 81–91.Google Scholar
Stearns, S.C. (1989) Trade-offs in life-history evolution. Functional Ecology 3, 259–268.Google Scholar
Stearns, S.C. (1992) The Evolution of Life Histories. Oxford, UK, Oxford University Press.Google Scholar
Stewart, L.A., Dixon, A.F.G., Ruzicka, Z. & Iperti, G. (1991a) Clutch and egg size in ladybird beetles. Entomophaga 36, 329–333.CrossRefGoogle Scholar
Stewart, L.A., Hemptinne, J.-L. & Dixon, A.F.G. (1991b) Reproductive tactics of ladybird beetles: relationships between egg size, ovariole number and developmental time. Functional Ecology 5, 380–385.CrossRefGoogle Scholar
Takakura, K.I. (2004) Variation in egg size within and among generations of the bean weevil, Bruchidius dorsalis (Coleoptera, Bruchidae): Effects of host plant quality and paternal nutritional investment. Annals of the Entomological Society of America 97, 346–352.CrossRefGoogle Scholar
Wilkinson, L.R. & Gibbons, J.W. (2005) Patterns of reproductive allocation: Clutch and egg size variation in three freshwater turtles. Copeia 4, 868–879.CrossRefGoogle Scholar
Williams, G.C. (1966) Adaptation and Natural Selection. Pinceton, NJ, USA, Princeton University Press.Google Scholar
Wright, E.J. & Laing, J.E. (1980) Numerical response of coccinellids to aphids in corn in southern Ontario. Canadian Entomologist 112, 977–988.CrossRefGoogle Scholar