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Specialist and generalist oviposition strategies in butterflies: maternal care or precocious young?

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Abstract

Herbivorous insects specialized on a narrow set of plants are believed to be better adapted to their specific hosts. This hypothesis is supported by observations of herbivorous insect species with a broader diet breadth which seemingly pay a cost through decreased oviposition accuracy. Despite many studies investigating female oviposition behavior, there is a lack of knowledge on how larvae cope behaviorally with their mothers’ egg-laying strategies. We have examined a unique system of five nymphalid butterfly species with different host plant ranges that all feed on the same host plant. The study of this system allowed us to compare at the species level how oviposition preference is related to neonate larval responses in several disadvantageous situations. We found a general co-adaptation between female and larval abilities, where species with more discriminating females had larvae that were less able to deal with a suboptimal initial feeding site. Conversely, relatively indiscriminate females had more precocious larvae with better abilities to cope with suboptimal sites. Despite similarities between the tested species with similar host ranges, there were also striking differences. Generalist and specialist species can be found side by side in many clades, with each clade having a specific evolutionary history. Such clade-specific, phylogenetically determined preconditions apparently have affected how precisely a broad or narrow diet breadth can be realized.

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References

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

    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  CAS  PubMed  Google Scholar 

  • Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Bernays EA, Wcislo WT (1994) Sensory capabilities, information processing, and resource specialization. Q Rev Biol 69:187–204

    Article  Google Scholar 

  • Bernays EA, Singer MS, Rodrigues D (2004) Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecol Entomol 29:389–397

    Article  Google Scholar 

  • Bryant SR, Thomas CD, Bale JS (2000) Thermal ecology of gregarious and solitary nettle-feeding nymphalid butterfly larvae. Oecologia 122:1–10

    Article  Google Scholar 

  • Carlsson MA, Bisch-Knaden S, Schäpers A, Mozuraitis R, Hansson BS, Janz N (2011) Odour maps in the brain of butterflies with divergent host-plant preferences. PLoS ONE 6:e24025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carlsson MA, Schäpers A, Nässel DR, Janz N (2013) Organization of the olfactory system of nymphalidae butterflies. Chem Senses 38:355–367

    Article  CAS  PubMed  Google Scholar 

  • Core Team R (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • De Bruyn L, Scheirs J, Verhagen R (2002) Nutrient stress, host plant quality and herbivore performance of a leaf-mining fly on grass. Oecologia 130:594–599

    Article  Google Scholar 

  • Doak P, Kareiva P, Kingsolver J (2006) Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology 87:395–408

    Article  PubMed  Google Scholar 

  • Dukas R (1998) Cognitive ecology––the evolutionary ecology of information processing and decision making. The University of Chicago Press, Chicago

    Google Scholar 

  • Ebert G (1993) Die Schmetterlinge Baden-Württembergs, Bd. 1, Tagfalter 1. Ulmer, Stuttgart

  • Egan SP, Funk DJ (2006) Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa. Proc R Soc B Biol Sci 273:843–848

    Article  Google Scholar 

  • Eliasson CU, Ryrholm N, Gärdenfors U (2005) Nationalnyckeln till Sveriges flora och fauna. Dagfjärilar: Hesperiidae-Nymphalidae. ArtDatabanken, Sveriges lantbruksuniversitet, Uppsala

    Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565

    Article  Google Scholar 

  • Friberg M, Olofsson M, Berger D, Karlsson B, Wiklund C (2008) Habitat choice precedes host plant choice––niche separation in a species pair of a generalist and a specialist butterfly. Oikos 117:1337–1344

    Article  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gamberale-Stille G, Söderlind L, Janz N, Nylin S (2014) Host plant choice in the comma butterfly–larval choosiness may ameliorate effects of indiscriminate oviposition. Insect Sci 21:499–506

    Article  PubMed  Google Scholar 

  • Hunter AF (1995) The ecology and evolution of reduced wings in forest macrolepidoptera. Evol Ecol 9:275–287

    Article  Google Scholar 

  • Janz N (2003) The cost of polyphagy: oviposition decision time vs error rate in a butterfly. Oikos 100:493–496

    Article  Google Scholar 

  • Janz N (2005) The relationship between habitat selection and preference for adult and larval food resources in the polyphagous butterfly Vanessa cardui (Lepidoptera : Nymphalidae). J Insect Behav 18:767–780

    Article  Google Scholar 

  • Janz N (2011) Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annu Rev Ecol Evol Syst 42:71–89

    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 B Biol Sci 264:701–707

    Article  Google Scholar 

  • Janz N, Nylin S (2008) The oscillation hypothesis of host-plant range and speciation. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, California, pp 203–215

    Google Scholar 

  • Janz N, Nyblom K, Nylin S (2001) Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini. Evolution 55:783–796

    Article  CAS  PubMed  Google Scholar 

  • Janz N, Söderlind L, Nylin S (2009) No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: nymphalidae): on the persistence of Hopkins’ host selection principle. Ecol Entomol 34:50–57

    Article  Google Scholar 

  • Joshi A, Thompson JN (1997) Adaptation and specialization in a two-resource environment in Drosophila species. Evolution 51:846–855

    Article  Google Scholar 

  • Kelber A (1999) Ovipositing butterflies use a red receptor to see green. J Exp Biol 202:2619–2630

    PubMed  Google Scholar 

  • Murphy SM (2004) Enemy-free space maintains swallowtail butterfly host shift. Proc Natl Acad Sci USA 101:18048–18052

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nylin S (1988) Host plant specialization and seasonality in a polyphagous butterfly, Polygonia c-album (Nymphalidae). Oikos 53:381–386

    Article  Google Scholar 

  • Nylin S, Janz N (1996) Host plant preferences in the comma butterfly (Polygonia c-album): do parents and offspring agree? Ecoscience 3:285–289

    Google Scholar 

  • Pullin AS (1987) Changes in leaf quality following clipping and regrowth of Urtica dioica, and consequences for a specialist insect herbivore, Aglais urticae. Oikos 49:39–45

    Article  Google Scholar 

  • Reavey D (1992) Egg size, first instar behaviour and the ecology of Lepidoptera. J Zool 227:277–297

    Article  Google Scholar 

  • Salama HS, Dimetry NZ, Salem SA (1971) On the host preference and biology of the cotton leaf worm Spodoptera littoralis Bois. Z Angew Entomol 67:261–266

    Article  Google Scholar 

  • Seppänen EJ (1970) Suurperhostoukkien ravintokasvit. Werner Söderström Osakeyhtiö, Helsinki

    Google Scholar 

  • Stamp NE (1980) Egg deposition patterns in butterflies: why do some species cluster their eggs rather than deposit them singly? Am Nat 115:367–380

    Article  Google Scholar 

  • Stefanescu C (1997) Migration patterns and feeding resources of the painted lady butterfly, Cynthia cardui (L.) (Lepidoptera, Nymphalidae) in the northeast of the Iberian peninsula. Miscell Zool 20:31–48

    Google Scholar 

  • Stefanescu C (2001) The nature of migration in the red admiral butterfly Vanessa atalanta: evidence from the population ecology in its southern range. Ecol Entomol 26:525–536

    Article  Google Scholar 

  • Thomas J, Lewington R (2010) Butterflies of Britain and Ireland. British Wildlife, Gillingham

    Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Tolman T, Lewington R (1997) Collins butterfly guide. HarperCollins, London

    Google Scholar 

  • Weingartner E, Wahlberg N, Nylin S (2006) Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae). J Evol Biol 19:483–491

    Article  CAS  PubMed  Google Scholar 

  • Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparancy and abundance of their host plants. Oecologia 63:23–29

    Article  Google Scholar 

  • Wiklund C, Friberg M (2008) Enemy-free space and habitat-specific host specialization in a butterfly. Oecologia 157:287–294

    Article  PubMed  Google Scholar 

  • Wiklund C, Persson A (1983) Fecundity, and the relation of egg weight variation to offspring fitness in the speckled wood butterfly Pararge aegeria, or why don’t butterfly females lay more eggs? Oikos 40:53–63

    Article  Google Scholar 

  • Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annu Rev Entomol 47:361–393

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Emilie Linderoth, Åsa Sandström and Julia Carlsson for assistance in the laboratory and Martin Olofsson for constructing the device to measure leaf toughness. The study was supported by a grant from the Faculty of Science, Stockholm University, to NJ and a grant from the Swedish Research Council (VR) to SN (Grant 2011-5636). We also acknowledge support from the Strategic Research Programme Ekoklim at Stockholm University.

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Correspondence to Alexander Schäpers.

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Communicated by Jennifer Thaler.

Why this study and paper deserves to be honored as a Highlighted Student Paper: Through a unique comparison between several butterfly species we cast new light on the costs of polyphagy, but also show that the “generalist” and “specialist” categories hide substantial variation. The co-adaptation of female choice and larval abilities on the species level cannot only be explained by the specialist-generalist axis, but can be properly understood in a historical framework.

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Schäpers, A., Nylin, S., Carlsson, M.A. et al. Specialist and generalist oviposition strategies in butterflies: maternal care or precocious young?. Oecologia 180, 335–343 (2016). https://doi.org/10.1007/s00442-015-3376-5

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  • DOI: https://doi.org/10.1007/s00442-015-3376-5

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