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A trade-off between female lifespan and larval diet breadth at the interspecific level in Lepidoptera

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Abstract

A prediction arising from several evolutionary diet breadth models is that, in insect herbivores whose adults practise adaptive host plant selection based on larval performance, female adult lifespan should be negatively correlated with larval diet breadth. In one category of models, female adult lifespan drives evolutionary changes in larval diet breadth; in the other category, larval diet breadth drives evolutionary changes in female adult lifespan. Applying the method of independent contrasts to a biologically and phylogenetically diverse array of Lepidoptera, we ask whether larval diet breadth—as measured by the number of larval food plant species reported in the literature—is negatively correlated with female adult lifespan at the interspecific level. We show that these two life history variables are indeed inversely related. Next, we relax the assumption, common to all of the models, that the female adult is the life stage responsible for the distribution of progeny among different host plants. By introducing into our data set three species whose females are incapable of flight (due to either aptery or brachyptery), and whose larvae are the dispersive stage, the negative correlation between female adult lifespan and larval diet breadth is lost, when using the independent contrasts method. We interpret this effect as supporting the models’ common prediction. Ours is the first reported evidence of a lifespan/diet breadth trade-off at the interspecific level among insects, and it confirms the findings of a previous study in which the degree of habitat specialisation among arthropods was inversely related to proxy measures of the degree of search time constraint. In one of our “diet breadth drives changes in lifespan” models, the females’ type of egg maturation strategy (as measured by the ovigeny index) is predicted to be positively correlated with larval diet breadth, and it mediates a female adult lifespan/larval diet breadth trade-off; however, we found no convincing support for such a role.

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References

  • Ballabeni P, Wlodarczyk M, Rahier M (2001) Does enemy-free space for eggs contribute to a leaf beetle’s oviposition preference for a nutritionally inferior host plant? Funct Ecol 15:318–324

    Article  Google Scholar 

  • Beccaloni GW, Symons FB (2000) Variation of butterfly diet breadth in relation to host-plant predictability: results from two faunas. Oikos 90:50–66

    Article  Google Scholar 

  • Berdegue M, Reitz SR, Trumble JT (1998) Host plant selection and development in Spodoptera exigua: do mother and offspring know best? Entomol Exp Appl 89:57–64

    Article  Google Scholar 

  • Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–727

    Article  PubMed  CAS  Google Scholar 

  • Björkman C, Larsson S, Bommarco R (1997) Oviposition preference in pine sawflies: a trade-off between larval growth and defence against natural enemies. Oikos 79:45–52

    Article  Google Scholar 

  • Bowden SR (1971) American white butterflies and English foodplants. J Lepid Soc 25:6–12

    Google Scholar 

  • Brower AVZ (2000) Phylogenetic relationships among the Nymphalidae (Lepidoptera) inferred from partial sequences of the wingless gene. Proc R Soc Lond B 267:1201–1211

    Article  CAS  Google Scholar 

  • Caterino MS, Reed RD, Kuo MM, Sperling FAH (2001) A partitioned likelihood analysis of swallowtail butterfly phylogeny (Lepidoptera: Papilionidae). Syst Biol 50:106–127

    Article  PubMed  CAS  Google Scholar 

  • Chew FS (1975) Coevolution of pierid butterflies and their cruciferous food plants. I. The relative quality of available resources. Oecologia 20:1117–1127

    Article  Google Scholar 

  • Courtney SP (1982) Coevolution of pierid butterflies and their cruciferous foodplants. II. Habitat selection, community structure and speciation. Oecologia 54:101–107

    Article  Google Scholar 

  • Cox CB, Moore PD (2005) Biogeography: an ecological and evolutionary approach. Blackwell Publishing, Oxford

    Google Scholar 

  • Denno RF, Larsson S, Olmstead KL (1990) Role of enemy-free space and plant quality in host-plant selection by willow beetles. Ecology 71:124–137

    Article  Google Scholar 

  • Ehrlich P, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Ellers J, van Alphen JJM (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. J Evol Biol 10:771–785

    Article  Google Scholar 

  • Ellers J, Jervis MA (2003) Body size and the timing of egg production in parasitoid wasps. Oikos 102:164–172

    Article  Google Scholar 

  • Ellers J, Jervis MA (2004) Why are so few parasitoid wasp species pro-ovigenic? Evol Ecol Res 6:937–1110

    Google Scholar 

  • Ellers J, Sevenster JG, Driessen G (2000) Egg load evolution in parasitoids. Am Nat 156:650–665

    Article  Google Scholar 

  • Fang QQ, Mitchell A, Regier JC, Mitter C, Friedlander TP, Poole RW (2000) Phylogenetic utility of the nuclear gene Dopa Decarboxylase in noctuoid moths (Insecta: Noctuoidea). Mol Phylogenet Evol 15:473–486

    Article  PubMed  CAS  Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defence. Rec Adv Phytochem 10:1–40

    CAS  Google Scholar 

  • Feldman TS, Haber WA (1998) Oviposition behavior, host plant use, and diet breadth of Anthanassa butterflies (Lepidoptera: Nymphalidae) using plants in the Acanthaceae in a Costa Rican community. Florida Entomol 81:396–406

    Article  Google Scholar 

  • Forister ML (2004) Oviposition preference and larval performance within a diverging lineage of lycaenid butterflies. Ecol Entomol 29:264–272

    Article  Google Scholar 

  • Fry JD (1996) The evolution of host specialization: are trade-offs overrated? Am Nat 148:S84–S107

    Article  Google Scholar 

  • Gaston KJ, Reavey D (1989) Patterns in the life histories and feeding strategies of British macrolepidoptera. Biol J Linn Soc 37:367–381

    Article  Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • Harvey P, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge

    Google Scholar 

  • Heimpel GE, Mangel M, Rosenheim JA (1998) Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field. Am Nat 152:273–289

    Article  PubMed  CAS  Google Scholar 

  • Heisswolf A, Obermaier E, Poethke J (2005) Selection of large plants for oviposition by a monophagous leaf beetle: nutritional quality or enemy-free-space. Ecol Entomol 30:299–306

    Article  Google Scholar 

  • Holling CS (1959a) The components of predation as revealed by a study of small mammal predation of the European sawfly. Can Entomol 91:293–320

    Google Scholar 

  • Holling CS (1959b) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Jaenike J (1978) On optimal oviposition behaviour in phytophagous insects. Theor Pop Biol 14:350–356

    Article  CAS  Google Scholar 

  • Jaenike J (1990) Host specialization by phytophagous insects. Ann Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Janz N, Nylin S (1997) The role of female search behaviour in determining host plant range in plant feeding insects: a test of the information processing hypothesis. Proc R Soc Lond B 264:710–707

    Article  Google Scholar 

  • Jervis MA, Ferns PN (2004) The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos 107:449–460

    Article  Google Scholar 

  • Jervis MA, Heimpel GE, Ferns PN, Harvey JA, Kidd NAC (2001) Life-history strategies in parasitoid wasps: a comparative analysis of ‘ovigeny’. J Anim Ecol 70:442–458

    Article  Google Scholar 

  • Jervis MA, Ferns PN, Heimpel GE (2003) Body size and the timing of egg production: a comparative analysis. Funct Ecol 17:375–383

    Article  Google Scholar 

  • Jervis MA, Boggs CL, Ferns PN (2005a) Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecol Entomol 30:359–375

    Article  Google Scholar 

  • Jervis MA Copland MJW, Harvey JA (2005b) The life cycle. In: Jervis MA (ed) Insects as natural enemies. Kluwer Academic Publishers, Dordrecht, pp 73–165

    Chapter  Google Scholar 

  • Jervis MA, Boggs CL, Ferns PN (2006) Egg maturation strategy and survival trade-offs in holometabolous insects: a comparative approach. Biol J Linn Soc (in press)

  • Johnson CG (1969) Migration and dispersal of insects by flight. Methuen, London

    Google Scholar 

  • de Jong R, Vane-Wright RI, Ackery PR (1996) The higher classification of butterflies (Lepidoptera): problems and prospects. Ent Scand 27:65–101

    Google Scholar 

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

    Article  Google Scholar 

  • Kawecki TJ (1994) Accumulation of deleterious mutations and the evolutionary cost of being a generalist. Am Nat 144:833–838

    Article  Google Scholar 

  • Kristensen NP, Skalski AW (1996) Phylogeny and palaeontology. In: Kristensen NP (ed) Lepidoptera, moths and butterflies. Walter de Gruyter, Berlin, pp 7–25

    Google Scholar 

  • Ladner DT, Altizer S (2005) Oviposition preference and larval performance of North American monarch butterflies on four Asclepias species. Ent Exp Appl 116:9–20

    Article  Google Scholar 

  • Levins R, MacArthur R (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911

    Article  Google Scholar 

  • Lewontin RC (1965) Selection for colonising ability. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 79–94

    Google Scholar 

  • Mangel M (1989) Evolution of host selection in parasitoids: does the state of the parasitoid matter? Am Nat 133:688–705

    Article  Google Scholar 

  • Mangel M, Roitberg B (1989) Dynamic information and host acceptance by a tephritid fly. Ecol Entomol 14:181–189

    Google Scholar 

  • May P (1988) Determinants of foraging profitability in two nectarivorous butterflies. Ecol Entomol 13:171–184

    Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • Minet J (1991) Tentative reconstruction of the ditrysian phylogeny (Lepidoptera: Glossata). Ent Scand 22:69–95

    Google Scholar 

  • Niemelä P, Hanhimäki S, Mannila R (1981) The relationship of adult size in noctuid moths (Lepidoptera, Noctuidae) to breadth of diet and growth form of plants. Ann Ent Fenn 47:17–20

    Google Scholar 

  • Obermaier E, Pfeiffer B, Linsenmair KE (2001) Mortality and parasitism in West African tortoise beetles (Coleoptera: Chrysomelidae). Entom General 25:189–203

    Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Prinzing A (2003) Are generalists pressed for time? An interspecific test of the time-limited disperser model. Ecology 84:1744–1755

    Google Scholar 

  • Renwick JAA (2002) The chemical world of crucivores: lures, treats and traps. Ent Exp Appl 104:35–42

    Article  CAS  Google Scholar 

  • Robinson GS (1999) HOSTS – a database of the hostplants of the world’s Lepidoptera. Nota Lep 22:35–47

    Google Scholar 

  • Robinson GS, Sattler K (2001) Plutella in the Hawaiian Islands – relatives and host races of the diamondback moth (Lepidoptera: Plutellidae). Occ Pap Bernice P Bishop Mus, Honolulu 67:1–27

    Google Scholar 

  • Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernández LM (2000) HOSTS – a database of the hostplants of the world’s Lepidoptera. http://www.nhm.ac.uk/entomology/hostplants/

  • Roitberg B (2000) Threats, flies, and protocol gaps: can evolutionary ecology save biological control? In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, New Jersey, pp 254–265

    Google Scholar 

  • Rosenheim JA (1996) An evolutionary argument for egg limitation. Evolution 50:2089–2094

    Article  Google Scholar 

  • Sahragard A, Jervis MA, Kidd NAC (1991) Influence of host availability on rates of oviposition and host-feeding, and on longevity in Dicondylus indianus Olmi (Hym., Dryinidae), a parasitoid of the Rice Brown Planthopper, Nilaparvata lugens Stål (Hem., Delphacidae). J Appl Entomol 112:153–162

    Article  Google Scholar 

  • Schoonhoven LM, Jermy T, van Loon JJA (1998) Insect-plant biology: from physiology to evolution. Chapman and Hall, London

    Google Scholar 

  • Sevenster JG, Ellers J, Driessen G (1998) An evolutionary argument for time limitation. Evolution 52:1241–1244

    Article  Google Scholar 

  • Singer MC, Ng D, Thomas CD (1988) Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977–985

    Article  Google Scholar 

  • Speight MR, Hunter MD, Watt AD (1999) Ecology of insects: concepts and applications. Blackwell, Oxford

    Google Scholar 

  • Stevens DJ, Hansell MH, Freel JA, Monaghan P (1999) Developmental trade-offs in caddis flies: increased investment in larval defence alters adult resource allocation. Proc R Soc Lond B 266:1049–1054

    Article  Google Scholar 

  • Stevens DJ, Hansell MH, Monaghan P (2000) Developmental trade-offs and life histories: strategic allocation of resources in caddis flies. Proc R Soc Lond B 267:1511–1515

    Article  CAS  Google Scholar 

  • Straatman R (1962) Notes on certain Lepidoptera ovipositing on plants which are toxic to their larvae. J Lepidop Soc 16:99–103

    Google Scholar 

  • Strauss SY, Zangerl AR (2002) Plant–insect interactions in terrestrial ecosystems. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 77–106

    Google Scholar 

  • Strong DR, Lawton JH, Southwood TRE (1984) Insects on plants: community patterns and mechanisms. Blackwell, Oxford

    Google Scholar 

  • Thorne AD, Pexton JJ, Dytham C, Mayhew PJ (2006) Small body size shifts development towards early reproduction in an insect. Proc R Soc Lond B 273:1099–1103

    Article  Google Scholar 

  • Wahlberg N, Weingartner E, Nylin S (2003) Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea). Mol Phylogenet Evol 28:473–484

    Article  PubMed  CAS  Google Scholar 

  • Wahlberg N, Braby MF, Brower AVZ, de Jong R, Lee M-M, Nylin S, Pierce N, Sperling FAH, Vila RU, Warren AD, Zhakarov E (2005) Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers. Proc R Soc Lond B 272:1577–1586

    Article  CAS  Google Scholar 

  • Wasserman SS, Mitter C (1978) The relationship of body size to breadth of diet in some Lepidoptera. Ecol Entomol 3:155–160

    Google Scholar 

  • Whitlock MC (1996) The Red Queen beats the jack-of-all trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am Nat 148:S65–S77

    Article  Google Scholar 

  • Wiklund C (1975) The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L.. Oecologia 18:186–197

    Article  Google Scholar 

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Acknowledgements

We thank: Gaden Robinson for advising us, on several occasions, on the “HOSTS” database and moth phylogenies; George Tordoff and Neil Kidd for very useful discussions; Fernley Symons for commenting on an early draft; George Heimpel for commenting on a late draft; Illik Saccheri for providing us with body mass data for Biston betularia; David Lees for advice on aspects of the biology of B. betularia and other moth species; both Peter Mayhew and an another, anonymous, reviewer for extremely valuable comments on the submitted manuscript.

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Correspondence to Mark A. Jervis.

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Jervis, M.A., Ferns, P.N. & Boggs, C.L. A trade-off between female lifespan and larval diet breadth at the interspecific level in Lepidoptera. Evol Ecol 21, 307–323 (2007). https://doi.org/10.1007/s10682-006-9102-3

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