Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T05:34:23.591Z Has data issue: false hasContentIssue false
  • English
  • Français

Coevolutionary fine-tuning: evidence for genetic tracking between a specialist wasp parasitoid and its aphid host in a dual metapopulation interaction

Published online by Cambridge University Press:  27 September 2011

F.N. Nyabuga ,
H.D. Loxdale ,
D.G. Heckel  and
W.W. Weisser
F.N. Nyabuga*
Affiliation:
Institute of Ecology, Friedrich Schiller University, Dornburger Strasse 159, 07743 Jena, Germany Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745 Jena, Germany
H.D. Loxdale
Affiliation:
Institute of Ecology, Friedrich Schiller University, Dornburger Strasse 159, 07743 Jena, Germany Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745 Jena, Germany
D.G. Heckel
Affiliation:
Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745 Jena, Germany
W.W. Weisser
Affiliation:
Institute of Ecology, Friedrich Schiller University, Dornburger Strasse 159, 07743 Jena, Germany
*
*Author for correspondence Fax: +46-40-46 21 66 E-mail: franklin.nyabuga@slu.se
Get access Rights & Permissions [Opens in a new window]

Abstract

In the interaction between two ecologically-associated species, the population structure of one species may affect the population structure of the other. Here, we examine the population structures of the aphid Metopeurum fuscoviride, a specialist on tansy Tanacetum vulgare, and its specialist primary hymenopterous parasitoid Lysiphlebus hirticornis, both of which are characterized by multivoltine life histories and a classic metapopulation structure. Samples of the aphid host and the parasitoid were collected from eight sites in and around Jena, Germany, where both insect species co-occur, and then were genotyped using suites of polymorphic microsatellite markers. The host aphid was greatly differentiated in terms of its spatial population genetic patterning, while the parasitoid was, in comparison, only moderately differentiated. There was a positive Mantel test correlation between pairwise shared allele distance (DAS) of the host and parasitoid, i.e. if host subpopulation samples were more similar between two particular sites, so were the parasitoid subpopulation samples. We argue that while the differences in the levels of genetic differentiation are due to the differences in the biology of the species, the correlations between host and parasitoid are indicative of dependence of the parasitoid population structure on that of its aphid host. The parasitoid is genetically tracking behind the aphid host, as can be expected in a classic metapopulation structure where host persistence depends on a delay between host and parasitoid colonization of the patch. The results may also have relevance to the Red Queen hypothesis, whereupon in the ‘arms race’ between parasitoid and its host, the latter ‘attempts’ to evolve away from the former.

Keywords

aphidMetopeurum fuscoviridehymenopterous parasitoidLysiphlebus hirticornistansy plantTanacetum vulgarespecialistgenetic variabilitygenetic trackingmetapopulation
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 2 , April 2012 , pp. 149 - 155
Copyright
Copyright © Cambridge University Press 2011

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

Althoff, D.M. & Thompson, J.N. (1999) Comparative geographic structures of two parasitoid-host interactions. Evolution 53, 818–825.Google ScholarPubMed
Anton, C., Zeisset, I., Musche, M., Durka, W., Boomsma, J.J. & Settele, J. (2007) Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape. Molecular Ecology 16, 3828–3838.Google Scholar
Brodmann, P.A., Wilcox, C.V. & Harrison, S. (1997) Mobile parasitoids may restrict the spatial spread of an insect outbreak. Journal of Animal Ecology 66, 65–72.Google Scholar
Dixon, A.F.G. (1998) Aphid Ecology. 2nd edn. London, UK, Chapman & Hall.Google Scholar
Ellner, S.P., McCauley, E., Kendall, B.E., Briggs, C.J., Hosseini, P.R., Wood, S.N., Janssen, A., Sabelis, M.W., Turchin, P., Nisbet, R.M. & Murdoch, W.W. (2001) Habitat structure and population persistence in an experimental community. Nature 412, 538–543.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, UK, Princeton University Press.Google Scholar
Goudet, J. (2002) FSTAT, A program to estimate and test gene diversities and fixation indices. Version 2.9.3. 2001. Available online at http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995) (accessed August 2011).Google Scholar
Hamilton, W.D. (1967) Extraordinary sex ratios. Science 156, 477–488.Google Scholar
Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service. Bmc Genetics 6, 1–6.CrossRefGoogle ScholarPubMed
Johannesen, J. & Seitz, A. (2003) Comparative population genetic structures of the fruit fly Urophora cardui and its primary parasitoid Eurytoma robusta. Entomologia Experimentalis et Applicata 108, 149–157.Google Scholar
Jones, T.H., Godfray, H.C.J. & Hassell, M.P. (1996) Relative movement patterns of a tephritid fly and its parasitoid wasps. Oecologia 106, 317–324.Google Scholar
Kankare, M., van Nouhuys, S., Gaggiotti, O. & Hanski, I. (2005) Metapopulation genetic structure of two coexisting parasitoids of the Glanville fritillary butterfly. Oecologia 143, 77–84.Google Scholar
Kraaijeveld, A.R. & Van Alphen, J.J.M. (1995) Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid specific components. Evolutionary Ecology 9, 10–17.Google Scholar
Kraaijeveld, A.R. & van der Wel, N.N. (1994) Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species. Ecological Entomology 19, 221–229.Google Scholar
Langella, O. (1999) POPULATIONS version 1.2.32. Available online at http://www.bioinformatics.org/project/?group_id=84 (accessed August 2011).Google Scholar
Loxdale, H.D., Hardie, J., Halbert, S., Foottit, R., Kidd, N.A.C. & Carter, C.I. (1993) The relative importance of short- and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society 68, 291–311.Google Scholar
Loxdale, H.D., Massonnet, B. & Weisser, W.W. (2010) Why are there so few aphid clones? Bulletin of Entomological Research 100, 613–622.Google Scholar
Loxdale, H.D., Lushai, G. & Harvey, J.A. (2011) The evolutionary improbability of ‘generalism’ in nature, with special reference to insects. Biological Journal of the Linnean Society 103, 1–18.Google Scholar
Loxdale, H.D., Schöfl, G., Wiesner, K.R., Nyabuga, N.N., Heckel, D.G. & Weisser, W.W.Stay at home aphids: comparative spatial and seasonal metapopulation structure and dynamics of two specialist tansy aphid species studied using microsatellite markers. Biological Journal of the Linnean Society 103, in press (doi: 10.1111/j.1095-8312.2011.01761.x.).Google Scholar
Mackauer, M. & Völkl, W. (2002) Brood-size and sex-ratio variation in field populations of three species of solitary aphid parasitoids (Hymenoptera: Braconidae, Aphidiinae). Oecologia 131, 296–305.Google Scholar
Massonnet, B. (2002) Metapopulation structure and population genetics of monophagous aphids on tansy (Tanacetum vulgare L.). PhD thesis, Naturwissenschaftlichen Fakultät Universität Basel, Basel, Switzerland.Google Scholar
Massonnet, B., Leterme, N., Simon, J.C. & Weisser, W.W. (2002) Characterization of microsatellite loci in the aphid species Metopeurum fuscoviride (Homoptera: Aphididae). Molecular Ecology Notes 2, 127–129.Google Scholar
Menken, S.B.J. (1991) Does haplodiploidy explain reduced levels of genetic variability in Hymenoptera? Proceedings of the Section: Experimental and Applied Entomology of the Netherlands Entomological Society (NEV) 2, 172–178.Google Scholar
Nyabuga, F.N., Loxdale, H.D., Sharbel, T.F., Todd, M. & Weisser, W.W. (2009) Microsatellites from Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae), a specialist primary parasitoid attacking the specialist tansy aphid, Metopeurum fuscoviride Stroyan (Hemiptera: Aphididae). Molecular Ecology Resources 9, 931–934.Google Scholar
Nyabuga, F.N., Loxdale, H.D., Heckel, D.G. & Weisser, W.W. (2010) Spatial population dynamics of a specialist aphid parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae: Aphidiinae): evidence for philopatry and restricted dispersal. Heredity 105, 433–442.Google Scholar
Nyabuga, F.N., Loxdale, H.D., Heckel, D.G. & Weisser, W.W. (2011) Temporal genetic structuring of a specialist parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae) attacking a specialist aphid on tansy. Biological Journal of the Linnean Society 102, 737–749.Google Scholar
Nyabuga, F.N., Völkl, W., Schwörer, U., Weisser, W.W. & Mackauer, M.Mating strategies in solitary aphid parasitoids: effect of patch residence time and ant attendance. Journal of Insect Behavior, in press (doi: 10.1007/s10905-011-9279-3).Google Scholar
Polaszek, A. (1986) The effects of two species of hymenopterous parasitoid on the reproductive system of the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 40, 285–292.Google Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Rauch, G. & Weisser, W.W. (2007) Local and spatial dynamics of a host-parasitoid system in a field experiment. Basic and Applied Ecology 8, 89–95.Google Scholar
Rousset, F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.Google Scholar
Sloggett, J.J. & Weisser, W.W. (2002) Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos 98, 323–333.Google Scholar
SPSS Inc. (2007) SPSS base 16.0 for windows user's guide. Chicago, IL, USA, SPSS Inc.Google Scholar
Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.Google Scholar
Taylor, L.R. (1974) Insect migration, flight periodicity and boundary layer. Journal of Animal Ecology 43, 225–238.Google Scholar
Thompson, J.N. (1994) The Coevolutionary Process. Chicago, IL, USA, University of Chicago.Google Scholar
van Valen, L. (1973) A new evolutionary law. Evolutionary Theory 1, 1–30.Google Scholar
Walton, M.P., Loxdale, H.D. & Allen-Williams, L.J. (2011) Flying with a ‘death sentence’ on board: electrophoretic detection of braconid parasitoid larvae in migrating winged grain aphids, Sitobion avenae (F.). Bulletin of Entomological Research 101, 443–449.Google Scholar
Wang, J.L. (2004) Application of the one-migrant-per-generation rule to conservation and management. Conservation Biology 18, 332–343.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Weisser, W.W. (2000) Metapopulation dynamics in an aphid-parasitoid system. Entomologia Experimentalis et Applicata 97, 83–92.Google Scholar
Weisser, W.W. & Härri, S.A. (2005) Colonisations and extinctions at multiple spatial scales: a case study in monophagous herbivores. Annales Zoologici Fennici 42, 363–377.Google Scholar
Wright, S. (1978) Evolution and Genetics of Populations: Variability within and among Natural Populations. Chicago, IL, USA, University of Chicago.Google Scholar
Zheng, C.Z., Weisser, W.W., Harri, S.A. & Ovaskainen, O. (2009) Hierarchical metapopulation dynamics of two aphid species on a shared host plant. American Naturalist 174, 331–341.Google Scholar