Prey species mediated slow and fast development in two aphidophagous ladybird beetles
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Abstract
Extensive research has explored how environmental factors impact the developmental rates of various organisms. However, the phenomenon of developmental rate polymorphism, where individuals within a cohort exhibit either slow or fast developmental rates under fluctuating environmental conditions, remains underexplored. In the current study, we investigated how different prey species (Aphis craccivora Koch, Aphis gossypii Glover, Aphis nerii Boyer de Fonscolombe, Lipaphis erysimi (Kaltenbach) and Rhopalosiphum maidis (Fitch)) affect the slow and fast development rates of two ladybird species, Cheilomenes sexmaculata (Fabricius) and Propylea dissecta (Mulsant), and how these rates influence their reproductive traits. We observed a distinct bimodal distribution pattern for each prey species, with two peaks representing the fast and slow developers. The distribution was skewed depending on the type of prey. Slow developers had a higher proportion of females, lived longer, and had lower body mass. On the other hand, fast-developing females had higher fecundity and egg viability. We observed a higher frequency of slow developers among beetles fed on A. nerii, L. erysimi, and R. maidis and fewer on A. craccivora and A. gossypii. We hypothesised that the observed variation in developmental rates at emergence is due to selective mortality influenced by the prey species, rather than differences in the developmental rates at egg laying. This study lays the groundwork for further research into developmental rate polymorphism, enhancing our understanding of its ecological and evolutionary causes, and aiding in the selection of fast-developing bioagents for biological pest control.
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References
Agarwala, B.K, Yasuda, H., & Sato, S. (2008). Life history response of a predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), to food stress. App. Entomol. Zool., 43: 183-189.
Arendt, J.D. (1997). Adaptive intrinsic growth rates: An integration across taxa. Quart. Rev. Biol., 72: 149-177.
Arijs, Y., & de Clercq, P. (2004). Liver-based arti?cial diets for the production of Orius laevigatus. Biocont., 49: 505-516.
Awmack, C.S., & Leather, S.R. (2007). Aphids as crop pests. Cromwell Press, Trowbridge. Pp: 717.
Bailey, K.M., & Houde, E.D. (1989). Predation on eggs and larvae of marine fishes and the problem of recruitment. Adv. J. Mar. Biol., 25: 1-83.
Benrey, B., & Denno, R.F. (1997). The slow-growth-high mortality hypothesis: a test using the cabbage butterfly. Ecology, 78(4): 987-999.
Bista, M., Mishra, G., & Omkar (2012). Influence of crowding and diet on the development and survival of the ladybird Brumoides suturalis (Coleoptera: Coccinellidae) reared on two aphid species. Int. J. Trop. Ins. Sci., 32(1): 64-68.
Bueno, J., & Lopez-Urrutia, A. (2012). The offspring-Development-Time/Offspring-Number Trade-Off. Am.Nat., 179: 6.
Chen, F., Xie, X., & Li, Z. (2012). Partial survival and extinction of a delayed predator-prey model with stage structure. Appl. Math. Comp., 219(8): 4157-4162.
Chippindale, A.K., Hoang, D.T., Service, P.M., & Rose, M.R. (1994). The evolution of development in Drosophila melanogaster selected for postponed senescence. Evol., 48:1880-1899.
Chown, S.L., & Gaston, K.J. (2010). Body size variation in insects: a macroecological perspective. Biol. Rev., 85: 139-169.
Cloutier, C., Duperron, J., Tertuliano, M., & McNeil, J.N. (2000). Host instar, body size and fitness in the koinobiotic
parasitiod Aphidius negripes. Entomol. Exp. et Applicata, 97: 29-40.
D’Amico, L.J., Davidowitz, G., & Nijhout, H.F. (2001). The
developmental and physiological basis of body size evolution
in an insect. Proc. R. Soc. Lond. B Biol. Sci., 268: 1589-1593.
Darwin, C. (1874). The descent of man and selection in relation to sex. 2nd ed. Appleton, New York.
Dixon, A.F.G. (2000). Insect Predator- Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press
Cambridge, U.K. pp. 257.
Dixon, A.F.G., & Guo, Y. (1993). Egg and cluster size in ladybird beetles (Coleoptera: Coccinellidae): The direct and indirect effects of aphid abundance. Eur. J. Entomol., 90: 457-463.
Fox, C.W., & Czesak, M.E. (2000). Evolutionary ecology of progeny size in arthropods. Ann. Rev. Entomol., 45: 341-369.
Francis, F., Haubruge, E., & Gasper, C. (2000). Influence of host plant on specialist/ generalist aphids on the development of Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol., 97: 481-485.
Garcia-Barros, E. (2000). Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidae, Hesperiodea). Biol. J. Linn. Soc., 70: 251-284.
Gouws, E.J., Gaston, K.J., & Chown, S.L. (2011). Intraspecific
Body Size Frequency Distributions of Insects. Plos One. 6(3): e16606.
Hanski, I., & Stahls, G. (1990). Prolonged diapause in fungivorous
Pegomya flies. Ecol. Entomol., 15: 241-244.
Hanski, I. (1988). Four kinds of extra long diapause: a review of theory and observations. Ann. Entomol. Fenn., 25: 37-53.
Helinski, M.E.H., & Harrington, L.C. (2011). Male mating history and body size influence female fecundity and
longevity of the dengue vector Aedes aegypti. J. Med. Entomol., 48(2): 202-211.
Henderson, S.A., & Albrecht, J.S.M. (1998). Abnormal and variable sex ratios in population samples of ladybirds. Biol.
J. Linn. Soc., 35: 275–296.
Hodek, I., Van Emden, H.F., & Honek, A. (2012). Ecology and behaviour of the ladybird beetles (Coccinellidae). A John
Wiley and Sons, Ltd., Publication U.K., pp 4229.
Hoffmann, A., & Parsons, P.A. (1989). An integrated approach
to environmental stress tolerance and life-history variation:
Desiccation tolerance in Drosophila. Biol. J. Linn. Soc ., 37:117-136.
Katvala, M., & Kaitala, A. (2001). Male choice for current female
fecundity in a polyandrous egg-carrying bug. Ani. Behav.,
: 133-137.
Kuzawa, C.W. (2005). Fetal origins of developmental plasticity:
Are fetal cues reliable predictors of future nutritional
environments? Am. J. Hum. Biol., 17: 5-21.
Kuzawa, C.W. (2008). The developmental origins of adult health: intergenerational inertia in adaptation and disease. In W. R.
Trevathan, E. O. Smith & J. J. McKenna (Eds.), Evolutionary Medicine and Health, pp. 325-349. New York: Oxford University Press.
Lazarevic, J., Tucic, N., Jovanovic, D.S., Vecera, J., & Kodrik,
D. (2012) The effects of selection for early and late
reproduction on metabolite pools in Acanthoscelides
obtectus Say. Ins. Sci., 19: 303-314.
Lewis, Z., Brakefield, P.M., & Wedell, N. (2010). Speed or sperm:
A potential trade-off between development and reproduction
in the butterfly, Bicyclus anynana (Lepidoptera:
Nymphalidae). Eur. J. Entomol., 107: 55-59.
Majerus, M.E.N. (1994). Ladybirds (New Naturalist Series).
HarperCollins, London. 367 pp.
Majerus, M.E.N. (2006). The impact of male-killing bacteria on
the evolution of aphidophagous coccinellids. Eur. J.
Entomol., 103: 1-7.
Maklakov, A.A., Bonduriansky, R. & Brooks, R.C. (2009). Sex
differences, sexual selection, and ageing: an experimental
approach. Evolution, 63: 2491-2503.
Marinkovic, D., Milosevic, M. & Milanovic, M. (1986). Enzyme
activity and dynamics of Drosophila development. Genet., 70: 43-52.
Michaud, J.P. (2005). On the assessment of prey suitability in
aphidophagous Coccinellidae. Eur. J. Entomol., 102: 385-390.
Miller, T.J., Crowder, L.B., Rice, J.A., & Marschall, E.A. (1988).
Larval size and recruitment mechanisms in fishes: toward a
conceptual framework. Can. J. Fish., Aqua., Sci., 45: 1657-1670.
Mishra, G., & Omkar (2012). Slow and Fast Development in
Ladybirds: Occurrence, Effects and Significance. Web Ecol.,
: 19-26.
Nyaanga, J.G., Kamau, A.W., Pathak, R.S., & Tuey, R.K. (2012). The effect of different cereal aphid species on the performance of two coccinellid predators. J. Entomol., 9:41-49.
Nowicki, P., Witek, M., Skorka, P., Settele, J., & Woyciechowski,
M. (2005). Population ecology of the endangered butterflies
Maculinea teleius and M. nausithous, and the implications
for conservation. Popul. Ecol., 47(3): 193-202.
Oli, M.K. (2004). The fast-slow continuum and mammalian
life-history patterns: An empirical evaluation. Basic App.
Ecol., 5: 449-463.
Omkar, & Afaq, U. (2013). Evaluation of Darwin’s fecundity
advantage hypothesis in Parthenium beetle, Zygogramma
bicolorata Pallister. Ins. Sci., 20: 531-540.
Omkar, & Mishra, G. (2005). Preference-performance of a
generalist predatory ladybird: a laboratory study. Biol. Cont., 34(2): 187-195.
Omkar, & Bind, R.B. (2004). Prey quality dependent growth,
development and reproduction of a biocontrol agent,
Cheilomenes sexmaculata (Fabricius) (Coleoptera:
Coccinellidae). Bio. Sci. Technol., 14(7): 665-673.
Omkar, & James, B.E. (2004). Influence of prey species on
immature survival, development, predation and reproduction
of Coccinella transversalis Fabricius (Col., Coccinellidae).
J. Appl. Entomol., 128(2): 150-157.
Omkar, & Pervez, A. (2003). Influence of prey deprivation on
biological attributes of pale morphs of the lady beetle
Propylea dissecta (Mulsant). Insect Science and its Application, 23(2): 143-148.
Omkar, Kumar, G., & Sahu, J. (2009). Performance of a predatory ladybird beetle, Anegleis cardoni (Coleoptera: Coccinellidae) on three aphid species. Eur. J., Entomol., 106: 565-572.
Omkar, Kumar, G., & Sahu,, J. (2011). Monotypic prey-mediated development, survival and life table attributes of a ladybird beetle Anegleis cardoni (Coleoptera: Coccinellidae) on different aphid species. Int.J.Trop.Ins.Sci., 31(3): 162-173.
Omkar, Sahu, J., & Kumar, G. (2010). Effect of prey quantity on reproductive and developmental attributes of a ladybird beetle, Anegleis cardoni. Int. J. Trop. Ins. Sci., 30(1): 48-56.
Osawa, N. (2000). Population field studies on the aphidophagous ladybird beetle Harmaonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Pop. Ecol., 42: 115-127.
Osawa, N., & Ohashi, K. (2008). Sympatric coexistence of sibling species Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae) and the roles of maternal investment through egg and sibling cannibalism. Eur. J. Entomol., 105: 445–454.
Pandey, P., Mishra, G., & Omkar (2013). Slow and fast development in Parthenium beetle and its effect on reproductive attributes. J. Asia Pac. Entomol., 16(4): 395-399.
Pappas, M.L., Broufas, G.D., & Koveos, D.S. (2007). Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae). Biol. Cont., 43: 163–170.
Partridge, L., & Fowler, K. (1992). Direct and correlated responses to selection on at age reproduction in Drosophila melanogaster. Evol., 46: 76-91.
Perry, J.C., & Roitberg, B.D. (2005). Ladybird mothers mitigate offspring starvation risk by laying trophic eggs. Behav. Ecol. Sociobiol., 58, 578-586.
Pervez, A., & Omkar (2004). Temperature-Dependent Life Attributes of an Aphidophagous Ladybird, Propylea dissecta. Bio. Sci. Technol., 14: 587-594.
Phoofolo, M.W., Elliott, NC., & Giles, K.L. (2009). Analysis of growth and development in the final instar of three species of predatory Coccinellidae under varying prey availability. Entomol. Exp. et Applicata, 131(3): 264-277.
Phoofolo, M.W., Giles, K.L., & Elliott, N.C. (2008). Larval life history responses to food deprivation in three species of predatory lady beetles (Coleoptera: Coccinellidae). Environ. Entomol., 37: 315-322.
Plaistow, S.J., Tsuchida, K., Tsubaki, Y., & Setsuda, K. (2005).
The effect of a seasonal time constraint on development time, body size, condition, and morph determination in the horned beetle Allomyrina dichotoma L (Coleoptera: Scarabaeidae). Ecol. Entomol., 30: 692-699.
Promislow, D.E.L., & Bugbee, M. (2000). Direct and correlated responses to selection on age at physiological maturity in Drosophila simulans. J. Evol. Biol., 13: 955–966.
Rhamhalinghan, M. (1985). Intraspecific variations in ovariole number / ovary in Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ind. Zool., 9: 91-97.
Roff, D.A. (2002). Life history evolution. Sunderland, MA: Sinauer.
Roper, C., Pignatelli, P., & Partridge, L. (1993). Evolutionary effects of selection on age at reproduction in larval and adult Drosophila melanogaster. Evol., 47: 445-455.
Santos-Cividanes, T.M., dos Anjos, A.C.R., Cividanes, F.J., & Dias, P.C. (2011). Effects of food deprivation on the development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae). Neotrop. Entomol., 40(1).
Sevenster, J.G., & Van Alphen, J.J. (1993). A life history tradeoff in Drosophila species and community structure in variable environments. J. Ani. Ecol., 62: 720-736.
Scannapieco, A.C., Sambucetti, P., & Norry, F.M. (2009). Direct and correlated responses to selection for longevity in Drosophila buzzatii. Biol. J. Linn. Soc., 97: 738-748.
Service, P.M. (1987). Physiological mechanisms of increased stress resistance in Drosophila melanogaster selected for postponed senescence. Physiol. Zool., 60: 321-326.
Singh, N., Mishra, G., & Omkar (2014). Does temperature modify slow and fast development in two aphidophagous ladybirds? J. Therm. Biol., 39: 24-31.
Skorping, A. (2007). Selecting for fast and slow maturing worms. Proc. R. Soc. L., 22(274): 1465-1466.
Sloggett, J.J., & Lorenz, M.W. (2008). Egg composition and reproductive investment in aphidophagous ladybird beetles (Coccinellidae: Coccinellini): egg development and interspecific variation. Physiol. Entomol., 33: 200-208.
Stearns, S.C. (1992). The Evolution of Life Histories. Oxford,
Oxford University Press.
Stern, D.L. (2010). Evolution, Development, and the Predictable Genome. Greenwood Village, Colorado, Roberts and Company Publishers.
Stillwell, R.C., Blanckenhorn, W.U., Teder, T., Davidowitz, G., & Fox, C.W. (2010). Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Ann. Rev. Entomol., 55: 227-245.
Stillwell, R.C., Morse, G.E., & Fox, C.W. (2007). Geographic variation in body size and sexual size dimorphism of a seedfeeding beetle. Am. Nat., 170: 358-369.
Tauber, C.A., Tauber, M.J., & Tauber, M.J. (1991). Egg size and
taxon their influence on survival and development of
chrysopid hatchlings after food and water-deprivation. Can.
J. Zool.-Revue Canadienne De Zoologie 69, 2644-2650.
Thomas, J.A., Elmes, W., & Wardlaw, J.C. (1998). Polymorphic
growth in larvae of the butterfly Maculinea rebeli, a social
parasite of Myrmica ant colonies. Proc. Biol. Sci., 265: 1895-1901.
Van Der Werf, W., Evans, E.W., & Powell, J. (2000). Measuring and modeling the dispersal of Coccinella septempunctata (Coleoptera: Coccinellidae) in alfalfa fields. Eur. J. Entomol., 97: 487-493.
Vivan, L.M., Torres, J.B., & Veiga, A.F.S.L. (2003). Development and reproduction of a predatory stink-bug, Podisus nigrispinus, in relation to two different prey types and environmental conditions. Biocontrol, 48: 155-168.
Walker, R., Gurven, M., Hill, K., Migliano, A, Chagnon, N., & De Souza R, (2006). Growth rates and life histories in twenty-two small-scale societies. Am. J. Hum., Biol., 18:295-311.
Williams, A.C., & Flaxman, S.M. (2012). Can predators assess the quality of their prey’s resource? Ani. Behav. 83(4): 883-890.
Witek, M., Sliwinska, E.B., Skorka, P., Nowicki, P., Settele, J., & Woyciechowski, M. (2006) Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects. Oecologia, 148: 729-733.