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Have Genetic Trade-Offs in Host Use been Overlooked in Arthropods?

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Abstract

A popular hypothesis to explain the high degree of host specialisation observed among mites and insects is the existence of host-associated fitness trade-offs. According to this theory, adaptation to a host results in a relatively poorer performance on alternative hosts due to the antagonistic pleiotropic action of one or more genes. Evidence in favour of the genetic trade-off hypothesis is however scarce. Recent ecological work has shown that the optimisation of adult performance drives the evolution of host choice in at least some phytophagous insects. Yet, most ecological and evolutionary studies on host choice assume that females maximise their fitness by optimising offspring performance. In this paper, we investigate whether a general lack of attention for the role of adult performance in host choice may have diminished the chance of detecting genetic trade-offs. We reviewed the literature on genetic trade-offs and showed that most studies neglected host specific variation in adult performance. Moreover, studies that considered both adult and offspring performance had a higher chance of detecting genetic fitness trade-offs. Our results also suggested that studies on asexual reproducing species tend to detect trade-offs more often than studies on obligate sexual reproducing species. We argue that future studies on genetic trade-offs should take all fitness parameters into account in order to be conclusive. This approach may reveal (i) that genetic trade-offs are more common than hitherto reported and/or (ii) that genetic trade-offs are more common, or more easily detected among asexual reproducing species like mites and aphids.

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References

  • A.A. Agrawal (2000) ArticleTitleHost-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts Ecology 81 500–508

    Google Scholar 

  • C.S. Awmack S.R. Leather (2002) ArticleTitleHost plant quality and fecundity in herbivorous insects Annu. Rev. Entomol. 47 817–844 Occurrence Handle10.1146/annurev.ento.47.091201.145300 Occurrence Handle11729092

    Article  PubMed  Google Scholar 

  • P. Ballabeni M. Rahier (2000) ArticleTitleA quantitative genetic analysis of leaf beetle larval performance on two natural hosts: including a mixed diet J. Evol. Biol. 13 98–106 Occurrence Handle10.1046/j.1420-9101.2000.00144.x

    Article  Google Scholar 

  • P. Ballabeni K. Gotthard A. Kayumba M. Rahier (2003) ArticleTitleLocal adaptation and ecological genetics of host-plant specialization in a leaf beetle Oikos 101 70–78 Occurrence Handle10.1034/j.1600-0706.2003.12569.x

    Article  Google Scholar 

  • E.A. Bernays (1991) ArticleTitleEvolution of insect morphology in relation to plants Phil. Trans. R. Soc. Lond. B. 333 257–264

    Google Scholar 

  • E.A. Bernays M. Graham (1988) ArticleTitleOn the evolution of host specificity in phytophagous arthropods Ecology 69 886–892

    Google Scholar 

  • R. Bultin (1987) ArticleTitleA new approach to sympatric speciation Trends Ecol. Evol. 2 310–311 Occurrence Handle10.1016/0169-5347(87)90085-1

    Article  Google Scholar 

  • P.P. Caballero C.C. Ramirez H.M. Niemeyer (2001) ArticleTitleSpecialisation pattern of the aphid Rhopalosiphum maidis is not modified by experience on a novel host Entomol. Exp. Appl. 100 43–52 Occurrence Handle10.1023/A:1019298732711

    Article  Google Scholar 

  • J.C. Carolina Herr M.W. Johnson (1992) ArticleTitleHost plant preference of Liriomyza sativae (Diptera, Agromyzidae) populations infesting green onion in Hawaii Environ. Entomol. 21 1097–1102

    Google Scholar 

  • Y. Carrière B.D. Roitberg (1994) ArticleTitleTrade-offs in responses to host plants within a population of a generalist herbivore, Choristoneura rosaceana Entomol. Exp. Appl. 72 173–180

    Google Scholar 

  • S.P. Carroll H. Dingle S.P. Klassen (1997) ArticleTitleGenetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug Evolution 51 1182–1188

    Google Scholar 

  • S.P. Courtney T.T. Kibota (1989) Mother doesn’t know best: selection of hosts by ovipositing insects E.A. Bernays (Eds) Insect–Plant Interactions NumberInSeries II. CRC Press Boca Raton 161–188

    Google Scholar 

  • P.W. Jong Particlede J.K. Nielsen (2002) ArticleTitleHost plant use of Phyllotreta nemorum: do coadapted gene complexes play a role Entomol. Exp. Appl. 104 207–215 Occurrence Handle10.1023/A:1021268611744

    Article  Google Scholar 

  • V.G. Dethier (1954) ArticleTitleEvolution of feeding preference in phytophagous insects Evolution 8 33–54

    Google Scholar 

  • A.E. Douglas (1997) ArticleTitleProvenance, experience and plant utilisation by the polyphagous aphid, Aphis fabae Entomol. Exp. Appl. 83 161–171 Occurrence Handle10.1023/A:1002986120223

    Article  Google Scholar 

  • M. Drès J. Mallet (2002) ArticleTitleHost races in plant-feeding insects and their importance in sympatric speciation Phil. Trans. R. Soc. Lond. B. 357 471–492 Occurrence Handle10.1098/rstb.2002.1059

    Article  Google Scholar 

  • J.A. Endler (2000) Adaptive genetic variation in the wild T.A. Mousseau B. Sinervo J.A. Endler (Eds) Adaptive Genetic Variation in the Wild Oxford University Press Oxford 251–260

    Google Scholar 

  • W.J. Etges (1993) ArticleTitleGenetics of host-cactus response and life-history evolution among ancestral and derived populations of cactophilic Drosophila mojavensis Evolution 47 750–767

    Google Scholar 

  • D.S. Falconer T.F.C. Mackay (1996) Introduction to Quantitative Genetics Longman Essex

    Google Scholar 

  • C.W. Fox (1993) ArticleTitleA quantitative genetic analysis of oviposition preference and larval performance on two hosts in the bruchid beetle, Callosobruchus maculatus Evolution 47 166–175

    Google Scholar 

  • C.W. Fox R.L. Caldwell (1994) ArticleTitleHost-associated fitness trade-offs do not limit the evolution of␣diet breadth in the small milkweed bug Lygaeus kalmii (Hemiptera: Lygaeidae) Oecologia 97 382–389

    Google Scholar 

  • C.W. Fox K.J. Waddell T.A. Mousseau (1994) ArticleTitleHost-associated fitness variation in a seed beetle (Coleoptera: Bruchidae): evidence for local adaptation to a poor quality host Oecologia 99 329–336 Occurrence Handle10.1007/BF00627746

    Article  Google Scholar 

  • L.R. Fox P.A. Morrow (1981) ArticleTitleSpecialization: species property or local phenomenon? Science 211 887–893

    Google Scholar 

  • J.D. Fry (1990) ArticleTitleTrade-offs in fitness on different hosts: evidence from a selection experiment with a phytophagous mite Am. Nat. 136 569–580 Occurrence Handle10.1086/285116

    Article  Google Scholar 

  • J.D. Fry (1992) ArticleTitleThe mixed-model analysis of variance applied to quantitative genetics: biological meaning of the parameters Evolution 46 540–550

    Google Scholar 

  • J.D. Fry (1993) ArticleTitleThe “general vigor” problem: Can antagonistic pleiotropy be detected when genetic covariances are positive? Evolution 47 327–333

    Google Scholar 

  • J.D. Fry (1996) ArticleTitleThe evolution of host specialization: are trade-offs overrated? Am. Nat. 148 S84–S107 Occurrence Handle10.1086/285904

    Article  Google Scholar 

  • J.D. Fry (2003) ArticleTitleDetecting ecological trade-offs using selection experiments Ecology 84 1672–1678

    Google Scholar 

  • D.J. Futuyma T.E. Philippi (1987) ArticleTitleGenetic variation and covariation in response to host plants by Alsophila pometaria (Lepidoptera: Geometridae) Evolution 41 269–279

    Google Scholar 

  • F. Gould (1979) ArticleTitleRapid host range evolution in a population of the phytophagous mite Tetranychus urticae Koch Evolution 33 791–802

    Google Scholar 

  • H. Gu A. Cao G.H. Walter (2001) ArticleTitleHost selection and utilisation of Sonchus oleraceus (Asteraceae) by Helicoverpa armigera (Lepidoptera: Noctuidae): a genetic analysis Ann. Appl. Biol. 138 293–299

    Google Scholar 

  • J.D. Hare G.G. Kennedy (1986) ArticleTitleGenetic variation in plant-insect associations: survival of Leptinotarsa decemlineata populations on Solanum carolinense Evolution 40 1031–1043

    Google Scholar 

  • D.J. Hawthorne S. Via (2001) ArticleTitleGenetic linkage of ecological specialization and reproductive isolation in pea aphids Nature 412 904–907 Occurrence Handle10.1038/35091062 Occurrence Handle11528477

    Article  PubMed  Google Scholar 

  • J. Jaenike (1978) ArticleTitleOn optimal oviposition behaviour in phytophagous insects Theor. Pop. Biol. 14 350–356 Occurrence Handle10.1016/0040-5809(78)90012-6

    Article  Google Scholar 

  • J. Jaenike (1986) ArticleTitleFeeding behavior and future fecundity in Drosophila Am. Nat. 127 118–123 Occurrence Handle10.1086/284473

    Article  Google Scholar 

  • J. Jaenike (1989) ArticleTitleGenetic population structure of Drosophila tripunctata: patterns of variation and covariation of traits affecting resource use Evolution 43 1467–1482

    Google Scholar 

  • J. Jaenike (1990) ArticleTitleHost specialization in phytophagous insects Annu. Rev. Ecol. Syst. 21 243–273 Occurrence Handle10.1146/annurev.es.21.110190.001331

    Article  Google Scholar 

  • A.C. James J. Jakubczak M.P. Riley J. Jaenike (1988) ArticleTitleOn the causes of monophagy in Drosophila quineria Evolution 42 626–630

    Google Scholar 

  • A. Joshi J.N. Thompson (1995) ArticleTitleTrade-offs and the evolution of host specialization Evol. Ecol. 9 82–92 Occurrence Handle10.1007/BF01237699

    Article  Google Scholar 

  • D.N. Karowe (1990) ArticleTitlePredicting host range evolution: colonization of Coronilla varia by Colias philodice (Lepidoptera: Pieridae) Evolution 44 1637–1647

    Google Scholar 

  • M.C. Keese (1998) ArticleTitlePerformance of two monophagous leaf feeding beetles (Coleoptera: Chrysomelidae) on each other’s host plant: do intrinsic factors determine host plant specialization? J. Evol. Biol. 11 403–419 Occurrence Handle10.1007/s000360050096

    Article  Google Scholar 

  • J. Lazarević V. Perić-Mataruga J. Ivanović M Andjelković (1998) ArticleTitleHost plant effects on the genetic variation and correlations in the individual performance of the gypsy moth Funct. Ecol. 12 141–148 Occurrence Handle10.1046/j.1365-2435.1998.00166.x

    Article  Google Scholar 

  • J. Lazarević V. Perić-Mataruga B. Stojković N. Tucić (2002) ArticleTitleAdaptation of the gypsy moth to an unsuitable host plant Entomol. Exp. Appl. 102 75–86 Occurrence Handle10.1023/A:1015238812443

    Article  Google Scholar 

  • S.R. Leather (1988) ArticleTitleSize, reproductive potential and fecundity in insects: things aren’t as simple as they seem Oikos 51 386–389

    Google Scholar 

  • W.H. Lu P. Logan (1994) ArticleTitleGenetic-variation in oviposition between and within populations of Leptinotarsa decemlineata (Coleoptera, Chrysomelidae) Ann. Entomol. Soc. Am. 87 634–640

    Google Scholar 

  • W.H. Lu G.G. Kennedy F. Gould (1997) ArticleTitleGenetic variation in larval survival and growth and response to selection by colorado potato beetle (Coleoptera: Chrysomelidae) on tomato Environ. Entomol. 26 67–75

    Google Scholar 

  • A. Mackenzie (1996) ArticleTitleA trade-off for host plant utilization in the black bean aphid, Aphis fabae Evolution 50 155–162

    Google Scholar 

  • P.J. Mayhew (1997) ArticleTitleAdaptive patterns of host–plant selection by phytophagous insects Oikos 79 417–428

    Google Scholar 

  • P.J. Mayhew (2001) ArticleTitleHerbivore host choice and optimal bad motherhood Trends Ecol. Evol. 16 165–167 Occurrence Handle10.1016/S0169-5347(00)02099-1 Occurrence Handle11245932

    Article  PubMed  Google Scholar 

  • C. Metha N. Patel (1995) StatXact 3 for Windows. Statistical Software for Exact Nonparametric Inference CYTEL Software Corporation Cambridge, USA

    Google Scholar 

  • D.P. Pashley (1988) ArticleTitleQuantitative genetics, development, and physiological adaptation in host strains of fall armyworm Evolution 42 93–102

    Google Scholar 

  • G.B. Peppe C. Lomônaco (2003) ArticleTitlePhenotypic plasticity of Myzus persicae (Hemiptera: Aphididae) raised on Brassica oleracea L. var acephala (kale) and Raphanus sativus L. (radish) Genet. Mol. Biol. 26 189–194 Occurrence Handle10.1590/S1415-47572003000200012

    Article  Google Scholar 

  • M.D. Rausher (1984) ArticleTitleTradeoffs in performance on different hosts: evidence from within- and between-site variation in the beetle Deloyala guttata Evolution 38 582–595

    Google Scholar 

  • M.D. Rausher (1988) ArticleTitleIs coevolution dead? Ecology 69 898–901

    Google Scholar 

  • D.A. Roff (1997) Evolutionary Quantitative Genetics Chapman and Hall New York

    Google Scholar 

  • J. Scheirs L. Bruyn ParticleDe (2002) ArticleTitleIntegrating optimal foraging and optimal oviposition theory in plant–insect research Oikos 96 187–191 Occurrence Handle10.1034/j.1600-0706.2002.960121.x

    Article  Google Scholar 

  • J. Scheirs L. Bruyn ParticleDe R. Verhagen (2000) ArticleTitleOptimization of adult performance determines host choice in a grass miner Proc. R. Soc. Lond. B. 267 2065–2069 Occurrence Handle10.1098/rspb.2000.1250

    Article  Google Scholar 

  • J. Scheirs L. Bruyn ParticleDe R. Verhagen (2001) ArticleTitleA test of the C3–C4 hypothesis with two grass miners Ecology 82 410–421

    Google Scholar 

  • J. Scheirs T.G. Zoebisch D.J. Schuster L. Bruyn ParticleDe (2004) ArticleTitleOptimal foraging shapes host preference of a polyphagous leafminer Ecol. Entomol. 29 375–379 Occurrence Handle10.1111/j.0307-6946.2004.00600.x

    Article  Google Scholar 

  • P.M. Service M.R. Rose (1985) ArticleTitleGenetic covariation among life-history components: the effect of novel environments Evolution 39 943–945

    Google Scholar 

  • J.N. Thompson (1988) ArticleTitleEvolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects Entomol. Exp. Appl. 47 3–14 Occurrence Handle10.1007/BF00186709

    Article  Google Scholar 

  • J.N. Thompson (1994) The Coevolutionary Process University of Chicago Press Chicago

    Google Scholar 

  • J.N. Thompson (1996) ArticleTitleTrade-offs in larval performance on normal and novel hosts Entomol. Exp. Appl. 80 133–139 Occurrence Handle10.1007/BF00194742

    Article  Google Scholar 

  • J.N. Thompson W. Wehling R. Podolsky (1990) ArticleTitleEvolutionary genetics of host use in swallowtail butterflies Nature 344 148–150 Occurrence Handle10.1038/344148a0

    Article  Google Scholar 

  • N. Tucić S. Mikuljanac O. Stojković (1997) ArticleTitleGenetic variation and covariation among life history traits in populations Acanthoscelides obtectus maintained on different hosts Entomol. Exp. Appl. 85 247–256 Occurrence Handle10.1023/A:1003173813934

    Article  Google Scholar 

  • H. Ueno N. Fujiyama H. Katakura (1997) ArticleTitleGenetic basis for different host use in Epilachna pustulosa, a herbivorous ladybird beetle Heredity 78 277–283 Occurrence Handle10.1038/sj.hdy.6880880

    Article  Google Scholar 

  • H. Ueno N. Fujiyama K. Irie Y. Sato H. Katakura (1999) ArticleTitleGenetic basis for established and novel host plant use in a herbivorous ladybird beetle Epilachna vigintioctomaculata. Entomol. Exp. Appl. 91 245–250 Occurrence Handle10.1023/A:1003687417245

    Article  Google Scholar 

  • H. Ueno N. Fujiyama I. Yao Y. Sato H. Katakura (2003) ArticleTitleGenetic architecture for normal and novel host-plant use in two local populations of the herbivorous ladybird beetle, Epilachna pustulosa J. Evol. Biol. 16 883–895 Occurrence Handle10.1046/j.1420-9101.2003.00604.x Occurrence Handle14635903

    Article  PubMed  Google Scholar 

  • S. Via (1984) ArticleTitleThe quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among plants Evolution 38 896–905

    Google Scholar 

  • S. Via (1990) ArticleTitleEcological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems Annu. Rev. Entomol. 35 421–446 Occurrence Handle10.1146/annurev.en.35.010190.002225 Occurrence Handle2405772

    Article  PubMed  Google Scholar 

  • S. Via (1991) ArticleTitleThe genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones Evolution 45 827–852

    Google Scholar 

  • S. Via (2001) ArticleTitleSympatric speciation in animals: the ugly duckling grows up Trends Ecol. Evol. 16 381–390 Occurrence Handle10.1016/S0169-5347(01)02188-7 Occurrence Handle11403871

    Article  PubMed  Google Scholar 

  • S. Via R. Lande (1985) ArticleTitleGenotype-environment interactions and the evolution of phenotypic plasticity Evolution 39 505–522

    Google Scholar 

  • J.J. Windig (1997) ArticleTitleThe calculation and significance testing of genetic correlations across environments J. Evol. Biol. 10 853–874 Occurrence Handle10.1007/s000360050058

    Article  Google Scholar 

  • S. Yano J. Takabayashi A. Takafuji (2001) ArticleTitleTrade-offs in performance on different plants may not restrict the host plant range of the phytophagous mite, Tetranychus urticae Exp. Appl. Acarol. 25 371–381 Occurrence Handle10.1023/A:1017926017081 Occurrence Handle11603730

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745, Jena, Germany

    Jan Scheirs

  2. Evolutionary Biology Group, University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Kurt Jordaens & Luc De Bruyn

  3. Institute of Nature Conservation, Kliniekstraat 25, 1070, Brussels, Belgium

    Luc De Bruyn

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  1. Jan Scheirs
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Correspondence to Jan Scheirs.

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Scheirs, J., Jordaens, K. & De Bruyn, L. Have Genetic Trade-Offs in Host Use been Overlooked in Arthropods?. Evol Ecol 19, 551–561 (2005). https://doi.org/10.1007/s10682-005-2004-y

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