Hostname: page-component-7479d7b7d-k7p5g Total loading time: 0 Render date: 2024-07-08T11:57:22.846Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic variation and covariation of aphid life-history traits across unrelated host plants

Published online by Cambridge University Press:  01 July 2008

C. Vorburger  and
N. Ramsauer
C. Vorburger*
Affiliation:
Institute of Zoology, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
N. Ramsauer
Affiliation:
Institute of Zoology, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
*
*Author for correspondence Fax: +41 44 635 68 21 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotype×environment interactions with respect to hosts. Alternative explanations are discussed.

Keywords

cost of acquisitiongenetic correlationshost specializationlife-history evolutionMyzus persicaetrade-offs
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 6 , December 2008 , pp. 543 - 553
Copyright
Copyright © 2008 Cambridge University Press

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.)

References

Bell, G. (1984a) Measuring the cost of reproduction. I. The correlation structure of the life table of a plankton rotifer. Evolution 38, 300–313.Google ScholarPubMed
Bell, G. (1984b) Measuring the cost of reproduction. II. The correlation structure of the life tables of five freshwater invertebrates. Evolution 38, 314–326.CrossRefGoogle ScholarPubMed
Bell, G. (1986) Reply to Reznick et al. Evolution 40, 1344–1346.CrossRefGoogle ScholarPubMed
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the World's Crops: An Identification and Information Guide, 2nd edn. 466 pp. Chichester, UK, John Wiley and Sons.Google Scholar
Charlesworth, B. (1990) Optimization models, quantitative genetics, and mutation. Evolution 44, 520–538.CrossRefGoogle ScholarPubMed
Charmantier, A. & Garant, D. (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proceedings of the Royal Society B: Biological Sciences 272, 1415–1425.CrossRefGoogle ScholarPubMed
Dedryver, C.A., Hullé, M., Le Gallic, J.F., Caillaud, M.C. & Simon, J.C. (2001) Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia 128, 379–388.CrossRefGoogle ScholarPubMed
de Jong, G. & van Noordwijk, A.J. (1992) Acquisition and allocation of resources: genetic (co)variances, selection, and life histories. The American Naturalist 139, 749–770.CrossRefGoogle Scholar
Edwards, O.R. (2001) Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts. Entomologia Experimentalis et Applicata 100, 21–30.CrossRefGoogle Scholar
Falconer, D.S. & Mackay, T.F.C. (1996) Introduction to Quantitative Genetics, 4th edn. 464 pp. Harlow, UK, Longman.Google Scholar
Fry, J.D. (1996) The evolution of host specialization: are trade-offs overrated? The American Naturalist 148, S84–S107.CrossRefGoogle Scholar
Gwynn, D.M., Callaghan, A., Gorham, J., Walters, K.F.A. & Fellowes, M.D.E. (2005) Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proceedings of the Royal Society of London, Series B: Biological Sciences 272, 1803–1808.Google ScholarPubMed
Hales, D.F., Tomiuk, J., Wöhrmann, K. & Sunnucks, P. (1997) Evolutionary and genetic aspects of aphid biology: A review. European Journal of Entomology 94, 1–55.Google Scholar
Herzog, J., Müller, C.B. & Vorburger, C. (2007) Strong parasitoid-mediated selection in experimental populations of aphids. Biology Letters 3, 667–669.CrossRefGoogle ScholarPubMed
Hoffmann, A.A. & Merilä, J. (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends in Ecology & Evolution 14, 96–101.CrossRefGoogle ScholarPubMed
Hoffmann, A.A. & Parsons, P.A. (1991) Evolutionary Genetics and Environmental Stress. 284 pp. Oxford, UK, Oxford University Press.Google Scholar
Hoffmann, A.A. & Parsons, P.A. (1997) Consistent heritability changes under poor growth conditions. Trends in Ecology & Evolution 12, 460–461.CrossRefGoogle ScholarPubMed
Houle, D. (1991) Genetic covariance of fitness correlates – what genetic correlations are made of and why it matters. Evolution 45, 630–648.CrossRefGoogle ScholarPubMed
Houle, D. (1992) Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204.CrossRefGoogle ScholarPubMed
Houle, D., Hughes, K.A., Hoffmaster, D.K., Ihara, J., Assimacopoulos, S., Canada, D. & Charlesworth, B. (1994) The effects of spontaneous mutation on quantitative traits.1. variances and covariances of life-history traits. Genetics 138, 773–785.CrossRefGoogle Scholar
Jaenike, J. (1990) Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21, 243–273.CrossRefGoogle Scholar
Joshi, A. & Thompson, J.N. (1995) Trade-offs and the evolution of host specialization. Evolutionary Ecology 9, 82–92.CrossRefGoogle Scholar
Klingenberg, C.P. & Spence, J.R. (1997) On the role of body size for life-history evolution. Ecological Entomology 22, 55–68.CrossRefGoogle Scholar
Lande, R. (1976) The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genetical Research 26, 221–235.CrossRefGoogle Scholar
Lenski, R.E. & Service, P.M. (1982) The statistical analysis of population growth rates calculated from schedules of survivorship and fecundity. Ecology 63, 655–662.CrossRefGoogle Scholar
Lynch, M. & Walsh, B. (1998) Genetics and Analysis of Quantitative Traits. 980 pp. Sunderland, Massachusetts, USA, Sinauer.Google Scholar
Mackenzie, A. (1996) A trade-off for host plant utilization in the black bean aphid, Aphis fabae. Evolution 50, 155–162.CrossRefGoogle ScholarPubMed
Papura, D., Simon, J.C., Halkett, F., Delmotte, F., Le Gallic, J.F. & Dedryver, C.A. (2003) Predominance of sexual reproduction in, Romanian populations of the aphid Sitobion avenae inferred from phenotypic and genetic structure. Heredity 90, 397–404.CrossRefGoogle ScholarPubMed
Peppe, F.B. & Lomônaco, C. (2003) Phenotypic plasticity of Myzus persicae (Hemiptera: Aphididae) raised on Brassica oleracea L. var. acephala (kale) and Raphanus sativus L. (radish). Genetics and Molecular Biology 26, 189–194.CrossRefGoogle Scholar
Reznick, D., Nunney, L. & Tessier, A. (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends in Ecology & Evolution 15, 421–425.CrossRefGoogle ScholarPubMed
Rispe, C., Simon, J.C. & Pierre, J.S. (1996) Fitness comparison between clones differing in their ability to produce sexuals in the aphid Rhopalosiphum padi. Entomologia Experimentalis et Applicata 80, 469–474.CrossRefGoogle Scholar
Robertson, A. (1959) The sampling variance of the genetic correlation coefficient. Biometrics 15, 469–485.CrossRefGoogle Scholar
Roff, D.A. (2000) Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence. Journal of Evolutionary Biology 13, 434–445.CrossRefGoogle Scholar
Scheiner, S.M. (1993) Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24, 35–68.CrossRefGoogle Scholar
Schmidt, D.D., Kessler, A., Kessler, D., Schmidt, S., Lim, M., Gase, K. & Baldwin, I.T. (2004) Solanum nigrum: A model ecological expression system and its tools. Molecular Ecology 13, 981–995.CrossRefGoogle Scholar
Schmidt, M.H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. & Tscharntke, T. (2003) Relative importance of predators and parasitoids for cereal aphid control. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 1905–1909.CrossRefGoogle ScholarPubMed
Service, P.M. & Lenski, R.E. (1982) Aphid genotypes, plant phenotypes, and genetic diversity: a demographic analysis of experimental data. Evolution 36, 1276–1282.CrossRefGoogle ScholarPubMed
Service, P.M. & Rose, M.R. (1985) Genetic covariation among life-history components – the effect of novel environments. Evolution 39, 943–945.CrossRefGoogle ScholarPubMed
Simons, A.M. & Roff, D.A. (1996) The effect of a variable environment on the genetic correlation structure in a field cricket. Evolution 50, 267–275.CrossRefGoogle Scholar
Spitze, K. (1995) Quantitative genetics of zooplankton life-histories. Experientia 51, 454–464.CrossRefGoogle Scholar
Tessier, A.J., Leibold, M.A. & Tsao, J. (2000) A fundamental trade-off in resource exploitation by Daphnia and consequences to plankton communities. Ecology 81, 826–841.CrossRefGoogle Scholar
van Noordwijk, A.J. & de Jong, G. (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. The American Naturalist 128, 137–142.CrossRefGoogle Scholar
Via, S. (1991) The genetic structure of host plant adaptation in a spatial patchwork – demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827–852.CrossRefGoogle Scholar
von Burg, S., Ferrari, J., Müller, C.B. & Vorburger, C. (2008) Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae – no evidence for trade-offs. Proceedings of the Royal Society of London, Series B 275, 1089–1094.Google ScholarPubMed
Vorburger, C. (2005) Positive genetic correlations among major life-history traits related to ecological success in the aphid Myzus persicae. Evolution 59, 1006–1015.Google ScholarPubMed
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19, 97–107.CrossRefGoogle ScholarPubMed
Vorburger, C., Lancaster, M. & Sunnucks, P. (2003a) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two ‘superclones’ in Victoria, Australia. Molecular Ecology 12, 3493–3504.CrossRefGoogle ScholarPubMed
Vorburger, C., Sunnucks, P. & Ward, S.A. (2003b) Explaining the coexistence of asexuals with their sexual progenitors: no evidence for general-purpose genotypes in obligate parthenogens of the peach-potato aphid, Myzus persicae. Ecology Letters 6, 1091–1098.CrossRefGoogle Scholar
Weber, G. (1985) Genetic variability in host plant adaptation of the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 38, 49–56.CrossRefGoogle Scholar
Weber, G. (1986) Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 40, 161–168.CrossRefGoogle Scholar
Wilson, A.C.C., Sunnucks, P., Blackman, R.L. & Hales, D.F. (2002) Microsatellite variation in cyclically parthenogenetic populations of Myzus persicae in south-eastern Australia. Heredity 88, 258–266.CrossRefGoogle ScholarPubMed