Skip to main content
Log in

The maintenance of intraspecific biodiversity: the interplay of selection on resource use and on natural enemy resistance in the pea aphid

  • Special Feature
  • Relationships between biodiversity and ecosystem functioning across different scales
  • Published:
Ecological Research

Abstract

Biodiversity has both intraspecific and interspecific components, and speciation is the process through which the former is converted to the latter. Ecological factors can cause population divergence and differentiation. In this paper, we investigate the interplay between top-down effects from natural enemies and bottom-up effects from host plants in an aphid model system. Pea aphids, Acyrthosiphon pisum, are known to form host-adapted races on Trifolium and Medicago. Here, replicate clones of pea aphids collected from a broader set of five host plant genera are screened for their performance on the same set of host plants and also for their resistance to four natural enemies: the parasitoids Aphidius eadyi and Aphidius ervi, and the entomopathogenic fungi Pandora (=Erynia) neoaphidis and Zoophthora phalloides. The populations showed clear adaptation to their host plant from which they were collected, but they also performed well on Vicia. Performance on the other three plant species was poor. The aphid population collected from Lotus was significantly better at defending itself against the parasitoid A. eadyi, and there was a tendency for the clones from Trifolium to be resistant to the pathogen P. neoaphidis. These patterns highlight the importance of understanding the ecological processes influencing speciation in the context of the web of ecological adaptations within which a species is embedded.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352

    Google Scholar 

  • Caillaud MC, Via S (2000) Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am Nat 156:606–621

    Article  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  PubMed  Google Scholar 

  • Eastop VF (1971) Keys for the identification of Acyrthosiphon (Hemiptera: Aphididae). Bull Br Mus nat Hist (Ent) 26:1–115

    Google Scholar 

  • Feder JL (1998) The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom. In: Howard DJ, Berlocher SH (eds) Endless forms species and speciation. Oxford University Press, New York, pp 130–144

    Google Scholar 

  • Fellowes MDE, Kraaijeveld AR, Godfray HCJ (1998) Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc R Soc London Ser B Biol Sci 265:1553–1558

    Article  Google Scholar 

  • Ferrari J, Godfray HCJ (2003) Resistance to a fungal pathogen and host plant specialization in the pea aphid. Ecol Lett 6:111–118

    Article  Google Scholar 

  • Ferrari J, Müller CB, Kraaijeveld AR, Godfray HCJ (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55:1805–1814

    PubMed  Google Scholar 

  • Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65

    Article  Google Scholar 

  • Gwynn DM, Callaghan A, Gorham J, Walters KFA, Fellowes MDE (2005) Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proc R Soc London Ser B Biol Sci 272:1803–1808

    Article  Google Scholar 

  • Hawthorne DJ, Via S (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904–907

    Article  PubMed  Google Scholar 

  • Heie OE (1994) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. V.E.J. Brill, Leiden

    Google Scholar 

  • Henter HJ, Via S (1995) The potential for coevolution in a host-parasitoid system. 1. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49:427–438

    Google Scholar 

  • Hufbauer RA, Via S (1999) Evolution of an aphid–parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53:1435–1445

    Google Scholar 

  • Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280

    Article  PubMed  Google Scholar 

  • Leonardo TE (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecol Lett 7:461

    Article  Google Scholar 

  • Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc London Ser B Biol Sci 29:61–65

    Google Scholar 

  • McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus) – evidence for a species pair in Paxton Lake, Texada Island, British Columbia. Can J Zool Rev Can Zool 70:361–369

    Google Scholar 

  • Milner RJ (1982) On the occurrence of pea aphids, Acyrthosiphon pisum, resistant to isolates of the fungal pathogen Erynia neoaphidis. Entomol Exp Appl 32:23–27

    Google Scholar 

  • Milner RJ (1985) Distribution in time and space of resistance to the pathogenic fungus Erynia neoaphidis in the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 37:235–240

    Article  Google Scholar 

  • Moran NA, Russell JA, Koga R, Fukatsu T (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71:3302–3310

    Article  PubMed  Google Scholar 

  • Nosil P (2004) Reproductive isolation caused by visual predation on migrants between divergent environments. Proc R Soc London Ser B Biol Sci 271:1521–1528

    Article  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    Article  PubMed  Google Scholar 

  • Polaszek A (1986) The effects of two species of hymenopterous parasitoid on the reproductive system of the pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 40:285–292

    Article  Google Scholar 

  • Reimchen TE (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus – an adaptation to predators. Can J Zool Rev Can Zool 58:1232–1244

    Google Scholar 

  • Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352

    Article  Google Scholar 

  • Rundle HD, Vamosi SM, Schluter D (2003) Experimental test of predation’s effect on divergent selection during character displacement in sticklebacks. Proc Natl Acad Sci USA 100:14943–14948

    Article  PubMed  Google Scholar 

  • Sandström J (1996) Temporal changes in host adaptation in the pea aphid, Acyrthosiphon pisum. Ecol Entomol 21:56–62

    Google Scholar 

  • Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947–955

    Article  Google Scholar 

  • Schluter D (1994) Experimental evidence that competition promotes divergence in adaptive radiation. Science 266:798–801

    Google Scholar 

  • Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380

    Article  PubMed  Google Scholar 

  • Schluter D (2003) Frequency dependent natural selection during character displacement in sticklebacks. Evolution 57:1142–1150

    PubMed  Google Scholar 

  • Simon JC, Carré S, Boutin M, Prunier-Leterme N, Sabater-Muñoz B, Latorre A, Bournoville R (2003) Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc R Soc London Ser B Biol Sci 270:1703–1712

    Article  Google Scholar 

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989–1989

    Article  PubMed  Google 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

    Google Scholar 

  • Via S (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446–1457

    Google Scholar 

  • Via S (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol Evol 16:381–390

    Article  PubMed  Google Scholar 

  • Via S, Hawthorne DJ (2005) Back to the future: genetic correlations, adaptation and speciation. Genetica 123:147–156

    Article  PubMed  Google Scholar 

  • Via S, Bouck AC, Skillman S (2000) Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54:1626–1637

    PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank S. Luzac and J. Toivonen for technical assistance, and D. Hawthorne, A. Kraaijeveld, C. Scarborough, F. van Veen and S. Via for helpful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia Ferrari.

About this article

Cite this article

Ferrari, J., Godfray, H.C.J. The maintenance of intraspecific biodiversity: the interplay of selection on resource use and on natural enemy resistance in the pea aphid. Ecol Res 21, 9–16 (2006). https://doi.org/10.1007/s11284-005-0136-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-005-0136-8

Keywords

Navigation