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Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis

The preference-performance hypothesis explains host specificity in phytophagous insects, positing that host plants chosen by adults confer the greatest larval fitness. However, adults sometimes oviposit on plants supporting low larval success because the components of host specificity (adult prefere...

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Autores principales: Greenstein, Lewis, Steele, Christen, Taylor, Caz M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9197062/
https://www.ncbi.nlm.nih.gov/pubmed/35700160
http://dx.doi.org/10.1371/journal.pone.0269701
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author Greenstein, Lewis
Steele, Christen
Taylor, Caz M.
author_facet Greenstein, Lewis
Steele, Christen
Taylor, Caz M.
author_sort Greenstein, Lewis
collection PubMed
description The preference-performance hypothesis explains host specificity in phytophagous insects, positing that host plants chosen by adults confer the greatest larval fitness. However, adults sometimes oviposit on plants supporting low larval success because the components of host specificity (adult preference, plant palatability, and larval survival) are non-binary and not necessarily correlated. Palatability (willingness to eat) is governed by chemical cues and physical barriers such as trichomes, while survival (ability to complete development) depends upon nutrition and toxicity. Absence of a correlation between the components of host specificity results in low-performance hosts supporting limited larval development. Most studies of specificity focus on oviposition behavior leaving the importance and basis of palatability and survival under-explored. We conducted a comprehensive review of 127 plant species that have been claimed or tested to be hosts for the monarch butterfly Danaus plexippus to classify them as non-hosts, low performance, or high performance. We performed a meta-analysis to test if performance status could be explained by properties of neurotoxic cardenolides or trichome density. We also conducted a no-choice larval feeding experiment to identify causes of low performance. We identified 34 high performance, 42 low performance, 33 non-hosts, and 18 species with unsubstantiated claims. Mean cardenolide concentration was greater in high- than low-performance hosts and a significant predictor of host status, suggesting possible evolutionary trade-offs in monarch specialization. Other cardenolide properties and trichome density were not significant predictors of host status. In the experiment, we found, of the 62% of larvae that attempted to eat low-performance hosts, only 3.5% survived to adult compared to 85% of those on the high-performance host, demonstrating that multiple factors affect larval host plant specificity. Our study is the first to classify all known host plants for monarchs and has conservation implications for this threatened species.
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spelling pubmed-91970622022-06-15 Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis Greenstein, Lewis Steele, Christen Taylor, Caz M. PLoS One Research Article The preference-performance hypothesis explains host specificity in phytophagous insects, positing that host plants chosen by adults confer the greatest larval fitness. However, adults sometimes oviposit on plants supporting low larval success because the components of host specificity (adult preference, plant palatability, and larval survival) are non-binary and not necessarily correlated. Palatability (willingness to eat) is governed by chemical cues and physical barriers such as trichomes, while survival (ability to complete development) depends upon nutrition and toxicity. Absence of a correlation between the components of host specificity results in low-performance hosts supporting limited larval development. Most studies of specificity focus on oviposition behavior leaving the importance and basis of palatability and survival under-explored. We conducted a comprehensive review of 127 plant species that have been claimed or tested to be hosts for the monarch butterfly Danaus plexippus to classify them as non-hosts, low performance, or high performance. We performed a meta-analysis to test if performance status could be explained by properties of neurotoxic cardenolides or trichome density. We also conducted a no-choice larval feeding experiment to identify causes of low performance. We identified 34 high performance, 42 low performance, 33 non-hosts, and 18 species with unsubstantiated claims. Mean cardenolide concentration was greater in high- than low-performance hosts and a significant predictor of host status, suggesting possible evolutionary trade-offs in monarch specialization. Other cardenolide properties and trichome density were not significant predictors of host status. In the experiment, we found, of the 62% of larvae that attempted to eat low-performance hosts, only 3.5% survived to adult compared to 85% of those on the high-performance host, demonstrating that multiple factors affect larval host plant specificity. Our study is the first to classify all known host plants for monarchs and has conservation implications for this threatened species. Public Library of Science 2022-06-14 /pmc/articles/PMC9197062/ /pubmed/35700160 http://dx.doi.org/10.1371/journal.pone.0269701 Text en © 2022 Greenstein et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Greenstein, Lewis
Steele, Christen
Taylor, Caz M.
Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title_full Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title_fullStr Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title_full_unstemmed Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title_short Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
title_sort host plant specificity of the monarch butterfly danaus plexippus: a systematic review and meta-analysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9197062/
https://www.ncbi.nlm.nih.gov/pubmed/35700160
http://dx.doi.org/10.1371/journal.pone.0269701
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