Abstract
Polyphagous butterflies, i.e., those that feed on multiple host plants, need to evolve adaptations against the defenses of many plants. Studies have focused on chemical defenses of host plants and counter-adaptations of their herbivores. Physical defenses, despite being the first line of defense of many plants, have received little attention. Grass feeding butterflies are among the most speciose adaptive radiations among insects. Grasses rely primarily on physical rather than chemical defenses. Therefore, it is interesting to understand how butterflies have adapted to grass feeding. Mandibles are the principal biting and chewing organs in insect larvae, and mandible morphology should affect the ability of butterflies to effectively feed on their host plants. We here ask whether grass feeding butterflies have plasticity in mandibular morphology to cope with grass physical defenses, using the widespread grass feeding butterfly Mycalesis mineus as a model. We first show that physical defenses of grasses, such as leaf toughness, presence of silica deposits and trichomes, negatively affect body size of the butterfly. Our results further indicate that larvae of M. mineus show mandible plasticity, with increased mandibular length and relative mass investment, when feeding on tougher leaves and leaves with silica deposits. We suggest that the evolution of mandible plasticity may have been a key component of the coevolutionary arms race between grasses and herbivorous insects. This plasticity may have also allowed butterflies such as M. mineus to colonize a broad range of habitats and geographic regions.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Acevedo FE, Peiffer M, Ray S et al (2021) Silicon-mediated enhancement of herbivore resistance in agricultural crops. Front Plant Sci. https://doi.org/10.3389/fpls.2021.631824
Akaike H (1983) Information measures and model selection. Proceedings of the 44th Session of the International Statistical Institute 50:277–291
Barbehenn RV, Bernays EA (1992) Relative nutritional quality of C3 and C4 grasses for a graminivorous lepidopteran, Paratrytone melane (Hesperiidae). Oecologia 92:97–103. https://doi.org/10.1007/BF00317268
Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493. https://doi.org/10.1086/650722
Bernays EA (1986) Diet-induced head allometry among foliage-chewing insects and its importance for graminivores. Science 231:495–497. https://doi.org/10.1126/science.231.4737.495
Bittencourt-Rodrigues R, Zucoloto F (2009) How feeding on young and old leaves affects the performance of Ascia monuste orseis (Godart) (Lepidoptera, Pieridae). Rev Bras Entomol. 5:35. https://doi.org/10.1590/S0085-56262009000100023
Cayssials V, Rodríguez C (2013) Functional traits of grasses growing in open and shaded habitats. Evol Ecol 27:393–407. https://doi.org/10.1007/s10682-012-9601-3
Dockter DE (1993) Developmental changes and wear of larval mandibles in Heterocampa guttivitta and Heterocampa subrotata (Notodontidae). J Lepidopterists Soc 47:32–48
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608. https://doi.org/10.2307/2406212
Frew A, Weston LA, Reynolds OL, Gurr GM (2018) The role of silicon in plant biology: a paradigm shift in research approach. Ann Bot 121:1265–1273. https://doi.org/10.1093/aob/mcy009
Godfrey GL, Miller JS, Carter DJ (1989) Two mouthpart modifications in Larval Notodontidae (Lepidoptera): their taxonomic distributions and putative functions. J NY Entomol Soc 97:455–470
Hartley SE, DeGabriel JL (2016) The ecology of herbivore-induced silicon defences in grasses. Funct Ecol 30:1311–1322. https://doi.org/10.1111/1365-2435.12706
Hauser M-T (2014) Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00320
Hochuli DF (1994) Nutritional ecology of herbivorous insects: studies on their functional morphology and the mechanical properties of plants. La Trobe University, Melbourne
Islam A, Razzak MA, Islam MH et al (2010) Dry and wet season polymorphism in the butterflies, Melanitis leda and Mycalesis mineus (Satyridae: Lepidoptera). Univ J Zool Rajshahi Univ 29:33–39
Janz N, Nylin S (2008) The oscillation hypothesis of host-plant range and speciation. Spec Speciat Radiat Evol Biol Herbiv Insects 2008:203–215
Jousselin E, Elias M (2019) Testing host-plant driven speciation in phytophagous insects : a phylogenetic perspective. ArXiv. Peer-reviewed and recommended by PCI Evolutionary Biology
Karban R, Takabayashi J (2019) Chewing and other cues induce grass spines that protect meristems. Arthropod-Plant Interact 13:541–550. https://doi.org/10.1007/s11829-018-9666-1
Kariyat RR, Balogh CM, Moraski RP et al (2013) Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae). Am J Bot 100:1014–1021. https://doi.org/10.3732/ajb.1200612
Kehimkar I (2008) The Book of Indian Butterflies. Bombay Natural History Society (India)
Khuliso E Ravhuhali (2021) Effect of soil type on spatial distribution and nutritive value of grass species growing in selected rangelands of South Africa: South African Journal of Plant and Soil: Vol 38, No 5. https://www.tandfonline.com/doi/abs/https://doi.org/10.1080/02571862.2021.1933630. Accessed 2 Nov 2022
Koo AJ, Arimura G (2022) Molecular biology of chemical defenses. Plant Mol Biol 109:351–353. https://doi.org/10.1007/s11103-022-01290-9
Koricheva J, Barton KE (2012) Temporal changes in plant secondary metabolite production: patterns, causes and consequences. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 34–55
Kursar TA, Dexter KG, Lokvam J et al (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci 106:18073–18078. https://doi.org/10.1073/pnas.0904786106
Lenth R, Singmann H, Love J, et al (2020) emmeans: Estimated marginal means, aka least-squares means
Linnaeus C (1758) Systema naturae. Vol.1. Ed.10. L. Salvii, Stockholm
Massey FP, Ennos AR, Hartley SE (2007) Herbivore specific induction of silica-based plant defences. Oecologia 152:677–683
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. https://doi.org/10.1146/annurev.es.11.110180.001003
Mbwile RP, Udén P (1997) Effects of age and season on growth and nutritive value of Rhodes grass (Chloris gayana cv. Kunth). Anim Feed Sci Technol 65:87–98. https://doi.org/10.1016/S0377-8401(96)01085-1
Molleman F, Halali S, Kodandaramaiah U (2020) Oviposition preference maximizes larval survival in the grass-feeding butterfly Melanitis leda (Lepidoptera: Nymphalidae). Eur J Entomol 117:1–17. https://doi.org/10.14411/eje.2020.001
Nitin R, Balakrishnan VC, Churi PV et al (2018) Larval host plants of the butterflies of the Western Ghats, India. J Threat Taxa 10:11495. https://doi.org/10.11609/jott.3104.10.4.11495-11550
Ohata M, Furumoto A, Ohsaki N (2011) Plastic changes in head size during juvenile development of the butterfly Pieris napi. Ecol Res 26:541–546. https://doi.org/10.1007/s11284-011-0811-x
Peña C, Wahlberg N (2008) Prehistorical climate change increased diversification of a group of butterflies. Biol Lett 4:274–278. https://doi.org/10.1098/rsbl.2008.0062
Peter A, Shanower T, Romeis J (1995) The role of plant trichomes in insect resistance: a selective review. Phytophaga 7:41–64
R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Rigby RA, Stasinopoulos DM (2005) Generalized additive models for location, scale and shape. J R Stat Soc Ser C Appl Stat 54:507–554. https://doi.org/10.1111/j.1467-9876.2005.00510.x
Safonkin AF, Triseleva TA, Yatsuk AA (2022) The role of grass biomes in diversification of phytophagous insects. Biol Bull Rev 12:S173–S181. https://doi.org/10.1134/S2079086422080072
Sahoo RK, Warren AD, Wahlberg N et al (2016) Ten genes and two topologies: an exploration of higher relationships in skipper butterflies (Hesperiidae). PeerJ 4:e2653. https://doi.org/10.7717/peerj.2653
Sahoo RK, Warren AD, Collins SC, Kodandaramaiah U (2017) Hostplant change and paleoclimatic events explain diversification shifts in skipper butterflies (Family: Hesperiidae). BMC Evol Biol 17:174. https://doi.org/10.1186/s12862-017-1016-x
Scheirs J, Bruyn LD, Verhagen R (2002) Seasonal changes in leaf nutritional quality influence grass miner performance. Ecol Entomol 27:84–93. https://doi.org/10.1046/j.1365-2311.2002.0378a.x
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Solofondranohatra CL, Vorontsova MS, Hackel J et al (2018) Grass functional traits differentiate forest and savanna in the madagascar central highlands. Front Ecol Evol 6:184. https://doi.org/10.3389/fevo.2018.00184
Stasinopoulos M, Rigby B, Akantziliotou C (2008) Instructions on how to use the gamlss package in R Second Edition
Thompson DB (1992) Consumption rates and the evolution of diet-induced plasticity in the head morphology of Melanoplus femurrubrum (Orthoptera: Acrididae). Oecologia 89:204–213. https://doi.org/10.1007/BF00317219
Tiple AD, Khurad AM (2009) Butterfly species diversity, habitats and seasonal distribution in and around Nagpur City, central India. World J Zool 4(3):153–162
Van Dam NM, De Jong TJ, Iwasa Y, Kubo T (1996) Optimal distribution of defences: are plants smart investors? Funct Ecol 10:128–136. https://doi.org/10.2307/2390271
War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
Whitman DW, Ananthakrishnan TN (2009) Phenotypic plasticity of insects: mechanisms and consequences. Enfield, NH, Science Publishers
Zunjarrao SS, Tellis MB, Joshi SN, Joshi RS (2019) Plant-insect interaction: the saga of molecular coevolution. In: Mérillon J-M, Ramawat KG (eds) Bioactive molecules in food. Springer International Publishing, Cham, pp 1–27
Zuur AF, Ieno EN (2016) A protocol for conducting and presenting results of regression-type analyses. Methods Ecol Evol 7:636–645. https://doi.org/10.1111/2041-210X.12577
Acknowledgements
The project was supported by intra-mural grants from Indian Institute of Science Education and Research Thiruvananthapuram (IISER TVM). I.P was supported by a research fellowship from IISER TVM. We thank Tarunkishwor Yumnam for help with the GAMLSS analysis.
Funding
This project was supported by intra-mural grants from Indian Institute of Science Education and Research Thiruvananthapuram (IISER TVM). I.P was supported by research fellowship from IISER TVM.
Author information
Authors and Affiliations
Contributions
IP conducted the experiments, analysed the data and wrote the manuscript. UK conceived and designed the experiments along with IP, and helped in the analyses and drafting of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethical approval
Formal consent was not required for this study.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Informed consent
Not Applicable.
Research involving human and animals rights
Not Applicable.
Additional information
Handling Editor: Dagmar Voigt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Prasannakumar, I., Kodandaramaiah, U. Adaptive phenotypic plasticity of mandibles with respect to host plants. Arthropod-Plant Interactions 18, 77–88 (2024). https://doi.org/10.1007/s11829-023-10013-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-023-10013-w