Abstract
The foraging behaviour of the salt-marsh parasitoid, Anagrus delicatus (Hymenoptera: Mymaridae), is distinguished by few eggs laid per patch of hosts and frequent dispersal among patches. We investigated the within-population genetic variability in six quantitative traits associated with this unusual behaviour: fecundity (lifetime number of eggs), time on a patch, number of ovipositions per patch, oviposition rate, ovipositor length and tibia length (a measure of body size). Forty-one wasp isolines were initiated from single parthenogenetic females from three isolated salt marshes, and were maintained for up to eight generations in the greenhouse. We estimated the genetic variance and broad-sense heritability (h2) of these traits and tested trait means for differences among isolines (genetic variation) and sites (geographical variation). We found significant genetic variability among isolines for all traits except oviposition rate. The behavioural and morphological traits had similar levels of genetic variance, indicating that the evolvability (ability to respond to selection) of the traits is similarly high. However, the behavioural traits had higher residual variances, resulting in lower heritabilities. Only two traits had significant heritabilities. Fecundity, which is probably a good proxy for fitness, ceteris paribus, varied from on average 26 to 40 eggs per isoline and had the highest h2, 0.47 ± 0.16 (mean ± SE). Ovipositor length had an h2 of 0.36 ± 0.17. These results suggest that the traits comprising the foraging strategy of A. delicatus should be amenable to selection (e.g. isolines could be selected that lay more eggs per host patch and consequently visit fewer patches). Genetic correlations among traits were numerous and positive. One important prediction from these data is that selection for larger wasps will result in large offspring with greater egg loads and higher oviposition rates. Wasps with this combination of attributes are likely to be more efficient natural enemies for use in biological control. In addition, there was no significant divergence (genetic or otherwise) in wasp morphology or behaviour among the three sites, even though they were separated by 8 km or more.
Similar content being viewed by others
Article PDF
References
Antolin, M F, and Strong, D R. 1987. Long-distance dispersal by a parasitoid (Anagrus delicatus, Mymaridae) and its host. Oecologia, 73, 288–292.
Ball, J C, and Dahlsten, D L. 1973. Hymenopterous parasites of Ips paraconfusus (Coleoptera: Scolytidae) larvae and their contribution to mortality. I. Influence of host tree and tree diameter on parasitization. Can Ent, 105, 1453–1464.
Becker, W A. 1984. Manual of Quantitative Genetics, 4th edn. Academic Enterprises, Pullman, WA.
Bouletrea, M. 1986. The genetic and coevolutionary interactions between parasitoids and their hosts. In: Waage, J. K. and Greathead, D. J. (eds) Insect Parasitoids, pp. 169–200. Academic Press, New York.
Bouskila, A, Robertson, I C, Robinson, M E, Roit-Berg, B D, Tenhumberg, B, Tyre, A J, Vanranden, E. 1995. Submaximal oviposition rates in a mymarid parasitoid: choosiness should not be ignored. Ecology, 76, 1990–1993.
Carton, Y, Capy, P, and Nappi, A J. 1989. Genetic variability of host-parasite relationship traits: utilization of isofemale lines in a Drosophila simulans parasitic wasp. Génét Sél Évol, 21, 437–446.
Carton, Y, and Nappi, A. 1991. The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecologica, 12, 89–104.
Charlesworth, B. 1984. The evolutionary genetics of life histories. In: Shorrocks, B. (ed) Evolutionary Ecology, pp. 117–133. Blackwell Scientific Publications, Oxford.
Charlesworth, B. 1987. The heritability of fitness. In: J. Bradbury and Andersson, M. (eds) Sexual Selection: Testing the Alternatives, pp. 21–40 Wiley, New York.
Charlesworth, D, and Charlesworth, B. 1987. Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst, 18, 237–268.
Charnov, E L, and Skinner, S W. 1988. Clutch size in parasitoids: the egg production rate as a constraint. Evol Ecol, 2, 167–174.
Chassain, C, and Bouletreau, M. 1987. Genetic variability in the egg-laying behavior of Trichogramma maidis. Entomophaga, 32, 149–157.
Chassain, C, and Bouletreau, M. 1991. Genetic variability in quantitative traits of host exploitation in Trichogramma (Hymenoptera: Trichogrammatidae). Genetica, 83, 195–202.
Crease, T J, Stanton, D J, and Hebert, P D N. 1989. Polyphyletic origins of asexuality in Daphnia pulex. II. Mitochondrial-DNA variation. Evolution, 43, 1016–1026.
Cronin, J T. 1991. Parasitoid Foraging Behavior and the Stabilization of Host-Parasitoid Populations. Ph.D. Thesis, Florida State University, Tallahassee, FL.
Cronin, J T, and Strong, D R. 1990. Biology of Anagrus delicatus (Hymenoptera: Mymaridae), an egg parasitoid of Prokelisia marginata (Homoptera: Delphacidae). Ann Entomol Soc Am, 83, 846–854.
Cronin, J T, and Strong, D R. 1993a. Substantially sub-maximal oviposition rates by a mymarid egg parasitoid in the laboratory and field. Ecology, 74, 1813–1825.
Cronin, J T, and Strong, D R. 1993b. Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae). Ecol Entomol, 18, 293–302.
Denno, R F, Schauff, M E, Wilson, S W, and Olmstead, K L. 1987. Practical diagnosis and natural history of two sibling salt marsh-inhabiting planthoppers (Homoptera: Delphacidae). Proc Entomol Soc Wash, 89, 687–700.
Falconer, D S. 1989. Introduction to Quantitative Genetics, 3rd edn. Longman, New York.
Godfray, H C J. 1987. Clutch size evolution in parasitic wasps. Am Nat, 129, 221–233.
Godfray, H C J. 1993. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ.
Godfray, H C J, and Ives, A R. 1988. Stochasticity in invertebrate clutch-size models. Theor Pop Biol, 33, 79–101.
Gustafsson, L. 1986. Lifetime reproductive success and heritability: empirical support for Fisher's fundamental theorem. Am Nat, 128, 761–764.
Hamilton, W D. 1967. Extraordinary sex ratios. Science, 156, 477–488.
Harshman, L G, and Futuyma, D J. 1985. The origin and distribution of clonal diversity in Alsophila pometaria (Lepidoptera: Geometridae). Evolution, 39, 315–324.
Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics, 130, 195–204.
Mangel, M. 1992. Descriptions of superparasitism by optimal foraging theory, evolutionarily stable strategies and quantitative genetics. Evol Ecol, 6, 152–169.
Mangel, M, and Clark, C W. 1988. Dynamic Modeling in Behavioral Ecology. Princeton University Press, Princeton, NJ.
Mollema, C. 1991. Heritability estimates of host selection behavior by the Drosophila parasitoid Asobara tabida. Neth J Zool, 41, 174–183.
Mousseau, T A, and Roff, D A. 1987. Natural selection and the heritability of fitness components. Heredity, 59, 181–197.
Nunney, L, and Luck, R F. 1988. Factors influencing the optimum sex ratio in a structured population. Theor Pop Biol, 33, 1–30.
Orzack, S H, and Gladstone, J. 1994. Quantitative genetics of sex ratio traits in the parasitic wasp, Nasonia vitripennis. Genetics, 137, 211–220.
Orzack, S H, and Parker, D E, Jr.. 1990. Genetic variation for sex ratio traits within natural populations of a parasitic wasp, Nasonia vitripennis. Genetics, 124, 373–384.
Parker, G A, and Courtney, S P. 1984. Models of clutch size in insect oviposition. Theor Pop Biol, 26, 27–48.
Prevost, G, and Lewis, W J. 1990. Heritable differences in the response of the braconid wasp Micropletis croceipes to volatile allelochemicals. J Insect Behav, 3, 277–287.
Price, T, and Schlüter, D. 1991. On the low heritability of life-history traits. Evolution, 45, 853–861.
Roderick, G K. 1987. Ecology and Evolution of Dispersal in Californian Populations of a Salt Marsh Insect, Prokelisia marginata. Ph.D. Thesis, University of California, Berkeley.
Roff, D A, and Mousseau, T A. 1987. Quantitative genetics and fitness: lessons from Drosophila. Heredity, 58, 103–118.
Rosenheim, J A, and Mangel, M. 1994. Patch leaving rules for parasitoids with imperfect host discrimination. Ecol Entomol, 19, 374–380.
Roughgarden, J. 1972. The evolution of niche width. Amer Natur, 106, 683–718.
SAS Institute, 1985. SAS Users Guide: Statistics, Version 5. SAS Institute, Cary, NC.
Searle, S R. 1971. Linear Models Wiley, New York.
Sequeira, R, and Mackauer, M. 1992a. Quantitative genetics of body size and development time in the parasitoid wasp Aphidus ervi (Hymenoptera: Aphididae). Can J Zool, 70, 1102–1108.
Sequeira, R, and Mackauer, M. 1992b. Covariance of adult size and development time in the parasitoid wasp Aphidus ervi in relation to the size of its host, Acyrthosiphon pisum. Evol Ecol, 6, 34–44.
Sokal, R R, and Rohlf, F J. 1981. Biometry, 2nd edn. Freeman, New York.
Spicher, D, and Josselyn, M. 1985. Spartina (Gramineae) in northern California: distribution and taxonomic notes. Madroño, 32, 158–167.
Stephens, D W, and Krebs, J R. 186. Foraging Theory. Princeton University Press, Princeton, NJ.
Stiling, P D, and Strong, D R. 1982. Egg density and the intensity of parasitism in Prokelisia marginata (Homoptera: Delphacidae). Ecology, 63, 1630–1635.
Stouthamer, R, and Luck, R F. 1993. Influence of microbe-associated parthenogenesis on the fecundity of Trichogramma deion and T. pretiosum. Entomologia exp appl, 67, 183–192.
Stouthhamer, R, and Werren, J H. 1993. Microbes associated with parthenogenesis in wasps of the genus Trichogramma. J Invert Path, 61, 6–9.
Strong, D R. 1988. Parasitoid theory: from aggregation to dispersal. Trends Ecol Evol, 3, 277–280.
Strong, D R. 1989. Density independence in space and inconsistent temporal relationships for host mortality caused by a fairyfly parasitoid. J Anim Ecol, 57, 1065–1076.
Taylor, P D, and Bulmer, M G. 1980. Local mate competition and the sex ratio. J Theor Biol, 86, 409–419.
Via, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution, 38, 896–905.
Visser, M E, Van Alphen, J J M, and Hemerik, L. 1992. Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. J Anim Ecol, 61, 93–101.
Wajnberg, E. 1993. Genetic variation in sex allocation in a parasitic wasp: variation in sex pattern within sequences of oviposition. Entomologia exp appl, 69, 221–229.
Wajnberg, E, Pizzol, J, and Babault, M. 1989. Genetic variation in progeny allocation in Trichogramma maidis. Entomologia exp appl, 53, 177–187.
Weis, A E, Abrahamson, W G, and McCrea, K D. 1985. Host gall size and oviposition success by the parasitoid Eurytoma gigantea. Ecol Entomol, 10, 341–348.
Werren, J H, Skinner, S W, and Huger, A M. 1986. Male-killing bacteria in a parasitic wasp. Science, 231, 990–992.
Williams, G C. 1975. Sex and Evolution. Princeton University Press, Princeton, NJ.
Wilson, C C, and Hebert, P D N. 1992. The maintenance of taxon diversity in an asexual assemblage: an experimental analysis. Ecology, 73, 1462–1472.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cronin, J., Strong, D. Genetics of oviposition success of a thelytokous fairyfly parasitoid, Anagrus delicatus. Heredity 76, 43–54 (1996). https://doi.org/10.1038/hdy.1996.6
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1996.6
Keywords
This article is cited by
-
Inheritance of an oviposition behavior by an egg parasitoid
Heredity (2002)