Stochasticity in reproductive opportunity and the evolution of egg limitation in insects

Evolution

Volumn 65, Issue 8, 2011, Pages 2300-2312

  Rosenheim, Jay A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bet hedging; Liebig's law; Life history evolution; Limiting factors; Oviposition behavior; Time limitation

Indexed keywords

EGG; EVOLUTIONARY BIOLOGY; FECUNDITY; INSECT; LIFE HISTORY TRAIT; LIMITING FACTOR; OVIPOSITION; POPULATION DYNAMICS; REPRODUCTIVE COST; SPATIOTEMPORAL ANALYSIS; STOCHASTICITY;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; ECOSYSTEM; EGG LAYING; EVOLUTION; FEMALE; FERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; OOCYTE; PHYSIOLOGY; POPULATION DYNAMICS; REPRODUCTION; STATISTICS; TIME;

ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; FEMALE; FERTILITY; INSECTS; MODELS, BIOLOGICAL; OVIPOSITION; OVUM; POPULATION DYNAMICS; REPRODUCTION; STOCHASTIC PROCESSES; TIME FACTORS;

HEXAPODA;

EID: 79960836757     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01305.x     Document Type: Article

References (72)

1. Alexander, R. M. 1997. A theory of mixed chains applied to safety factors in biological systems. J. Theor. Biol. 184:247-252.
2. Ashman, T.-L., T. M. Knight, J. A. Steets, P. Amarasekare, M. Burd, D. R. Campbell, M. R. Dudash, M. O. Johnston, S. J. Mazer, R. J. Mitchell, et al. 2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408-2421.
3. Babendreier, D., and T. S. Hoffmeister. 2002. Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate. Entomol. Exp. Appl. 105:63-69.
4. Begon, M., and G. A. Parker. 1986. Should egg size and clutch size decrease with age? Oikos 47:293-302.
5. Bernstein, C., and J. Jervis. 2008. Food-searching in parasitoids: the dilemma of choosing between 'immediate' or future fitness gains. Pp. 129-171 in E. Wajnberg, C. Bernstein and J. van Alphen, eds. Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell, Malden, MA.
6. Boggs, C. L. 2003. Environmental variation, life histories, and allocation. Pp. 185-206 in C. L. Boggs, W. B. Watt and P. R. Ehrlich, eds. Butterflies: ecology and evolution taking flight. Univ. of Chicago Press, Chicago, IL.
7. Burd, M., T.-L. Ashman, D. R. Campbell, M. R. Dudash, M. O. Johnston, T. M. Knight, S. J. Mazer, R. J. Mitchell, J. A. Steets, and J. C. Vamosi. 2009. Ovule number per flower in a world of unpredictable pollination. Am. J. Bot. 96:1159-1167.
8. Casas, J., R. M. Nisbet, S. Swarbrick, and W. W. Murdoch. 2000. Eggload dynamics and oviposition rate in a wild population of a parasitic wasp. J. Anim. Ecol. 69:185-193.
9. Casas, J., F. Vannier, N. Mandon, J. P. Delbecque, D. Giron, and J. P. Monge. 2009. Mitigation of egg limitation in parasitoids: immediate hormonal response and enhanced oogenesis after host use. Ecology 90:537-545.
10. Charnov, E. L., and S. W. Skinner. 1985. Complementary approaches to the understanding of parasitoid oviposition decisions. Environ. Entomol. 14:383-391.
11. Cohen, D. 1966. Optimizing reproduction in a randomly varying environment. J. Theor. Biol. 12:119-129.
12. Cohen, D., and R. Dukas. 1990. The optimal number of female flowers and the fruits-to-flowers ratio in plants under pollination and resources limitation. Am. Nat. 135:218-241.
13. Ellers, J., and M. A. Jervis. 2003. Body size and the timing of egg production in parasitoid wasps. Oikos 102:164-172.
14. Ellers, J., and M. A. Jervis. 2004. Why are so few parasitoid wasp species pro-ovigenic? Evol. Ecol. Res. 6:993-1002.
15. Ellers, J., J. G. Sevenster, and G. Driessen. 2000. Egg load evolution in parasitoids. Am. Nat. 156:650-665.
16. Gandon, S., J. Varaldi, F. Fleury, and A. Rivero. 2009. Host-parasitoid coexistence and egg-limited encounter rates. Evolution 63:2974-2984.
17. Getz, W. M., and N. J. Mills. 1996. Host-parasitoid coexistence and egg-limited encounter rates. Am. Nat. 148:333-347.
18. Gillespie, J. H. 1973. Polymorphism in random environments. Theor. Popul. Biol. 4:193-195.
19. Godfray, H. C. J. 1994. Parasitoids: behavioral and evolutionary ecology. Princeton Univ. Press, Princeton, NJ.
20. Haccou, P., and J. J. M. van Alphen. 2008. Competition and asymmetric wars of attrition in insect parasitoids. Pp. 193-211 in E. Wajnberg, C. Bernstein and J. van Alphen, eds. Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell, Malden, MA.
21. Haldane, J. B. S., and S. D. Jayakar. 1963. Polymorphism due to selection of varying direction. J. Genet. 58:237-242.
22. Hassell, M. P. 1978. The dynamics of arthropod predator-prey systems. Princeton Univ. Press, Princeton, NJ.
23. Hassell, M. P. 2000. The Spatial and temporal dynamics of host-parasitoid interactions. Oxford Univ. Press, Oxford, UK.
24. Heimpel, G. E., C. Neuhauser, and M. Hoogendoorn. 2003. Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecol. Lett. 6:556-566.
25. Hopper, K. R. 1999. Risk-spreading and bet-hedging in insect population biology. Ann. Rev. Entomol. 44:535-560.
26. Iwasa, Y., Y. Suzuki, and H. Matsuda. 1984. Theory of oviposition strategy of parasitoids. 1. Effect of mortality and limited egg number. Theor. Popul. Biol. 26:205-227.
27. Javois, J., and T. Tammaru. 2004. Reproductive decisions are sensitive to cues of life expectancy: the case of a moth. Anim. Behav. 68:249-255.
28. Jervis, M. A., and P. N. Ferns. 2004. The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos 107:449-460.
29. Jervis, M. A., Ellers, J., and Harvey, J. A. 2008. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53:361-385.
30. Jervis, M. A., C. L. Boggs, and P. N. Ferns. 2005. Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecol. Entomol. 30:359-375.
31. Jervis, M. A., P. N. Ferns, and C. L. Boggs. 2007. A trade-off between female lifespan and larval diet breadth at the interspecific level in Lepidoptera. Evol. Ecol. 21:307-323.
32. Kean, J., Wratten, S., Tylianakis, J., and Barlow, N. 2003. The population consequences of natural enemy enhancement, and implications for conservation biological control. Ecol. Lett. 6:604-612.
33. Knight, T. M., J. A. Steets, and T.-L. Ashman. 2006. A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. Am. J. Bot. 93:271-277.
34. Kon, R., and S. J. Schreiber. 2009. Multiparasitoid-host interactions with egg-limited encounter rates. SIAM J. Appl. Math. 69:959-976.
35. Lewontin, R. C., and D. Cohen. 1969. On population growth in a randomly varying environment. Proc. Natl. Acad. Sci. USA 62:1056-1060.
36. Lotka, A. J. 1925. Elements of physical biology. Williams & Wilkins Co, Baltimore, MD.
37. Mangel, M. 1987. Oviposition site selection and clutch size in insects. J. Math. Biol. 25:1-22.
38. Mangel, M. 1989. Evolution of host selection in parasitoids: does the state of the parasitoid matter? Am. Nat. 133:688-705.
39. Mangel, M., and G. E. Heimpel. 1998. Reproductive senescence and dynamic oviposition behaviour in insects. Evol. Ecol. 12:871-879.
40. MacArthur, R. H. 1972. Geographical ecology: patterns in the distribution of species. Harper & Row, New York.
41. Minkenberg, O. P. J. M., M. Tatar, and J. A. Rosenheim. 1992. Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65:134-142.
42. Murdoch, W. W., C. J. Briggs, and R. M. Nisbet. 2003. Consumer-resource dynamics. Princeton Univ. Press, Princeton, NJ.
43. Nicholson, A. J., and V. A. Bailey. 1935. The balance of animal populations. Proc. Zool. Soc. Lond. 3:551-598.
44. Papaj, D. R. 2000. Ovarian dynamics and host use. Annu. Rev. Entomol. 45:423-448.
45. Olofsson, H., J. Ripa, and N. Jonzén. 2009. Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proc. R. Soc. Lond. B 276:2963-2969.
46. Orr, H. A. 2007. Absolute fitness, relative fitness, and utility. Evolution 61:2997-3000.
47. Richard, R., and J. Casas. 2009. Stochasticity and controllability of nutrient sources in foraging: host-feeding and egg resorption in parasitoids. Ecol. Monogr. 79:465-483.
48. Roff, D. A. 2002. Life history evolution. Sinauer Associates, Sunderland, MA.
49. Roff, D. A. 2008. Defining fitness in evolutionary models. J. Genet. 87:339-348.
50. Roitberg, B. D., J. Sircom, C. A. Roitberg, J. J. M. van Alphen, and M. Mangel. 1993. Life expectancy and reproduction. Nature 364:108.
51. Roitberg, B. D., K. Zimmermann, and T. S. Hoffmeister. 2010. Dynamic response to danger in a parasitoid wasp. Behav. Ecol. Sociobiol. 64:627-637.
52. Rosenheim, J. A. 1996. An evolutionary argument for egg limitation. Evolution 50:2089-2094.
53. Rosenheim, J. A. 1999a. Characterizing the cost of oviposition in insects: a dynamic model. Evol. Ecol. 13:141-165.
54. Rosenheim, J. A. 1999b. The relative contributions of time and eggs to the cost of reproduction. Evolution 53:376-385.
55. Rosenheim, J. A., and D. Rosen. 1991. Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of egg load and experience. J. Anim. Ecol. 60:873-893.
56. Rosenheim, J. A., G. E. Heimpel, and M. Mangel. 2000. Egg maturation, egg resorption and the costliness of transient egg limitation. Proc. R. Soc. Lond. B 267:1565-1573.
57. Rosenheim, J. A., S. J. Jepsen, C. E. Matthews, D. S. Smith, and M. R. Rosenheim. 2008. Time limitation, egg limitation, the cost of oviposition, and lifetime reproduction by an insect in nature. Am. Nat. 172:486-496.
58. Rosenheim, J. A., U. Alon, and G. Shinar. 2010. Evolutionary balancing of fitness-limiting factors. Am. Nat. 175:662-674.
59. Sakai, S. 1996. On ovule production in environments where pollinator or resource availability is unpredictable. J. Theor. Biol. 183:317-327.
60. Schreiber, S. J. 2006. Host-parasitoid dynamics of a generalized Thompson model. J. Math. Biol. 52:719-732.
61. Schreiber, S. J. 2007. Periodicity, persistence, and collapse in host-parasitoid systems with egg limitation. J. Biol. Dyn. 1:273-288.
62. Schreiber, S. J., and M. Vejdani. 2006. Handling time promotes the coevolution of aggregation in predator-prey systems. Proc. R. Soc. Lond. B 273:185-191.
63. Sevenster, J. G., J. Ellers, and G. Driessen. 1998. An evolutionary argument for time limitation. Evolution 52:1241-1244.
64. Shea, K., R. M. Nisbet, W. W. Murdoch, and H. J. S. Yoo. 1996. The effect of egg limitation on stability in insect host-parasitoid population models. J. Anim. Ecol. 65:743-755.
65. Tentelier, C., E. Desouhant, and X. Fauvergue. 2006. Habitat assessment by parasitoids: mechanisms for patch use behavior. Behav. Ecol. 17:515-521.
66. Thompson, W. R. 1924. La théorie mathématique de l'action des parasites entomophages et le facteur du hasard. Annales Faculté des Sciences de Marseille, 2d ser. 2:69-89.
67. van Baalen, M. 2000. The evolution of parasitoid egg load. Pp. 103-120 in M. E. Hochberg and A. R. Ives, eds. Parasitoid population biology. Princeton Univ. Press, Princeton, NJ.
68. van Baalen, M., and L. Hemerik. 2008. Parasitoid fitness: from a simple idea to an intricate concept. Pp. 31-50 in E. Wajnberg, C. Bernstein and J. van Alphen, eds. Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell, Malden, MA.
69. Visser, M. E., J. J. M. van Alphen, and L. Hemerik. 1992. Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. J. Anim. Ecol. 61:93-101.
70. Wajnberg, É. 2006. Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav. Ecol. Sociobiol. 60:589-611.
71. West, S. A., and J. P. Cunningham. 2002. A general model for host plant selection in phytophagous insects. J. Theor. Biol. 214:499-513.
72. West, S. A., and A. Rivero. 2000. Using sex ratios to estimate what limits reproduction in parasitoids. Ecol. Lett. 3:294-299.