- Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States of America
- Behavior & Social Evolution, Expression Studies, Genotype-Phenotype, Molecular Evolution
Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato
Impact of pollen-feeding on egg-laying and cyanogenic glucoside abundance in red postman butterfliesRecommended by Adriana Briscoe based on reviews by Carol Boggs, Caroline Mueller and 1 anonymous reviewer
Growth, development and reproduction in animals are all limited by dietary nutrients. Expansion of an organism’s diet to sources not accessible to closely related species reduces food competition, and eases the constraints of nutrient-limited diets. Adult butterflies are herbivorous insects known to feed primarily on nectar from flowers, which is rich in sugars but poor in amino acids. Only certain species in the genus Heliconius are known to also feed on pollen, which is especially rich in amino acids, and is known to prolong their lives by several months. The ability to digest pollen in Heliconius has been linked to specialized feeding behaviors (Krenn et al. 2009) and extra-oral digestion using enzymes, possibly including duplicated copies of cocoonase (Harpel et al. 2016; Smith et al. 2016 and 2018), a protease used by some moths to digest silk upon eclosion from their cocoons. In this reprint, Pinheiro de Castro and colleagues investigated the impact of artificial and natural diets on egg-laying ability, body weight, and cyanogenic glucoside abundance in adult Heliconius erato butterflies of both sexes.
Previous studies (Dunlap-Pianka et al. 1981) in H. charithonia demonstrated that access to dietary pollen led to extended egg-laying ability among adult female butterflies compared to females deprived of pollen, and compared to Dryas iulia females which feed only on nectar. In the current study, Pinheiro de Castro et al. (2023) examine the impact of diet on both young and old H. erato, over a longer period of time than the earlier work, highlighting the importance of extending the time period over which effects are evaluated. In addition to extending egg-laying ability in older females, the authors found that pollen in the diet appeared to maintain older female body weight, presumably because the pollen contained nutrients depleted during egg-laying.
The authors then investigated the effects of nutrition on the production of cyanogenic glycoside defenses. Heliconius are aposematic butterflies that sequester cyanide-forming defense chemicals from food plants as larvae or synthesize these compounds de novo. The authors found the abundance of cyanogenic glycosides to be significantly greater in butterflies with access to pollen, but again only in older females.
Curiously, field studies of male and female H. charithonia butterflies found that females in the wild collected more pollen than males (Mendoza-Cuenca and Macías-Ordóñez 2005). Taken together, these new findings raise the intriguing possibility that females collect more pollen than males, in part, because pollen has a bigger impact on female survival and reproduction. A small limitation of the study is the use of wing length, rather than body weight, at the zero time point. But the trend is clear in both males and females, and it adds supporting detail to the efficacy of pollen feeding as an unusual strategy for increasing fertility and survival in Heliconius butterflies.
Dunlap-Pianka, Helen, Carol L. Boggs, Lawrence E. Gilbert. (1977) Ovarian dynamics in heliconiine butterflies: Programmed senescence versus eternal youth. Science, 197: 487-490, https://doi.org/10.1126/Science.197.4302.487
Pinheiro de Castro, Erika C., Josie McPherson, Glennis Julian, Anniina L. K. Mattila, Søren Bak, Stephen H. Montgomery, Chris Jiggins. (2023) Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato. bioRxiv, 2023.01.13.523799, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.01.13.523799
Krenn, Harald W., Monika J. B. Eberhard, Stefan H. Eberhard, Anna-Laetitia Hikl, Werner Huber, Lawrence E. Gilbert (2009). Mechanical damage to pollen aids nutrient acquisition in Heliconius butterflies (Nymphalidae). Arthropod-Plant Interactions, 3: 203–208. https://doi.org/10.1007/s11829-009-9074-7
Harpel, Desiree, Darron A. Cullen, Swidbert R. Ott, Chris D. Jiggins, James R. Walters (2015) Pollen feeding proteomics: Salivary proteins of the passion flower butterfly, Heliconius melpomene. Insect Biochemistry and Molecular Biology, 63: 7-13, https://doi.org/10.1016/j.ibmb.2015.04.004
Mendoza-Cuenca, Luis, Rogelio Macías-Ordóñez (2005) Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioral compensation. Journal of Tropical Ecology, 21: 407-415. https://doi.org/10.1017/S0266467405002385
Smith, Gilbert, Aide Macias-Muñoz, John Kelly, Carter Butts, Rachel Martin, Adriana D. Briscoe (2018) Evolutionary and structural analyses uncover a role for solvent interactions in the diversification of cocoonases in butterflies. Proceedings of the Royal Society B, 285: 20172037. https://doi.org/10.1098/rspb.2017.2037
Smith, Gilbert, Aide Macias-Muñoz, Adriana D. Briscoe (2016) Gene duplication and gene expression changes play a role in the evolution of candidate pollen-feeding genes in Heliconius butterflies. Genome Biology and Evolution, 8: 2581-2596. https://doi.org/10.1093/gbe/evw180