Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses
- Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, United States
- Department of Integrative Biology and Biodiversity Collections, University of Texas at Austin, United States
- Smithsonian Tropical Research Institute, Panama
- Grupo de Investigación en Ecología Evolutiva en los Trópicos (EETROP), Universidad de las Américas, Ecuador
- Ecological Networks Lab, Technische Universität Darmstadt, Germany
- Departamento de Ciencias Biológicas, Universidad de los Andes, Colombia
- Department of Biology, Stanford University, United States
- Max Planck Institute for Evolutionary Biology, Germany
- Department of Chemistry and Physics, Indiana State University, United States
- Museo de Zoología, Escuela de Biología, Facultad de Ciencias Exactas y Naturales, Pontificia Universidad Católica del Ecuador, Ecuador
- Department of Biological Sciences, St John’s University, United States
Figures
Figure 1
A new evolutionary model of toxin sequestration in Dendrobatidae.
We propose that alkaloid consumption, some level of alkaloid resistance, and passive accumulation were present in the most recent common ancestor of Dendrobatidae; enhanced resistance and …
Figure 2
From left to right: an ultrametric tree showing phylogenetic relationships inferred previously (Wan et al., 2023) among sampled species with the three defended poison frog clades highlighted in purple, the undefended clades in dark gray, and non-dendrobatids in light gray (Bufonidae: Amazophrynella siona and Atelopus aff. spurrelli; Leptodactylidae: Lithodytes lineatus).
Tile color indicates the log of the total quantity of alkaloids in each class as measured by the sum of integrated areas of alkaloids of that class from GC-MS data per individual. The number in each …
Figure 3
Hypothesized physiological processes that interact to determine the defense phenotype: toxin intake, toxin elimination (Elim.), and toxin sequestration (Seq.).
A new paradigm: the passive-accumulation hypothesis for definitions. Although toxin intake sets a maximum for the total possible amount of toxin accumulation (Acc.), it cannot fully explain the …
Tables
Table 1
Range and median of alkaloid quantity (estimated by the sum of integrated areas) and alkaloid diversity (number of different compounds) by species from the GC-MS assessment.
The presumed chemical defense phenotype for poison frogs is given according to Santos and Cannatella, 2011. Purple rows highlight defended species. *From a UHPLC-HESI-MS/MS dataset for which …
| Family | Subfamily | Species | Phenotype | Sample Size (frogs) | Log (Total Integrated Area) | Alkaloid Number | ||
|---|---|---|---|---|---|---|---|---|
| Range | Median | Range | Median | |||||
| Dendrobatidae | Aromobatinae | Rheobates palmatus | undefended | 4 | 13.07–14.24 | 14.00 | 1–4 | 1.5 |
| Dendrobatidae | Aromobatinae | Allobates insperatus | undefended | 8 | 13.47–15.44 | 14.99 | 1–9 | 5.0 |
| Dendrobatidae | Aromobatinae | Allobates juanii | undefended | 1 | 14.10 | 14.10 | 1 | 1.0 |
| Dendrobatidae | Aromobatinae | Allobates kingsburyi | undefended | 1 | 13.63 | 13.63 | 2 | 2.0 |
| Dendrobatidae | Aromobatinae | Allobates talamancae | undefended | 3 | 14.89–16.27 | 15.09 | 2–4 | 3.0 |
| Dendrobatidae | Aromobatinae | Allobates zaparo | undefended | 1 | 16.78 | 16.78 | 8 | 8.0 |
| Dendrobatidae | Colostethinae | Leucostethus fugax | undefended | 8 | 12.57–15.33 | 14.00 | 3–8 | 4.5 |
| Dendrobatidae | Colostethinae | Ameerega bilinguis | defended | 1 | 21.97 | 21.97 | 133 | 133.0 |
| Dendrobatidae | Colostethinae | Ameerega hahneli | defended | 4 | 20.21–22.29 | 21.68 | 85–140 | 128.5 |
| Dendrobatidae | Colostethinae | Silverstoneia flotator* | undefended | 12 | NA | NA | 0–1 | 0.0 |
| Dendrobatidae | Colostethinae | Silverstoneia aff. gutturalis | undefended | 9 | 11.80–17.33 | 15.40 | 1–10 | 3.0 |
| Dendrobatidae | Colostethinae | Silverstoneia erasmios | undefended | 2 | 14.70–16.11 | 15.41 | 15–15 | 15.0 |
| Dendrobatidae | Colostethinae | Epipedobates aff. espinosai | defended | 2 | 18.44–20.20 | 19.32 | 83–131 | 107.0 |
| Dendrobatidae | Colostethinae | Epipedobates anthonyi | defended | 1 | 20.54 | 20.54 | 127 | 127.0 |
| Dendrobatidae | Colostethinae | Epipedobates boulengeri | defended | 2 | 18.87–19.39 | 19.13 | 77–94 | 85.5 |
| Dendrobatidae | Colostethinae | Epipedobates currulao | defended | 2 | 19.49–19.68 | 19.59 | 99–105 | 102.5 |
| Dendrobatidae | Colostethinae | Epipedobates espinosai | defended | 2 | 18.82–21.33 | 20.08 | 85–146 | 115.5 |
| Dendrobatidae | Colostethinae | Epipedobates machalilla | defended | 2 | 12.98–15.67 | 14.32 | 8–38 | 23.0 |
| Dendrobatidae | Colostethinae | Epipedobates tricolor | defended | 2 | 18.36–19.07 | 18.72 | 91–114 | 102.5 |
| Dendrobatidae | Hyloxalinae | Hyloxalus awa | undefended | 7 | 0.00–16.05 | 13.58 | 0–12 | 3.0 |
| Dendrobatidae | Hyloxalinae | Hyloxalus shuar | undefended | 1 | 14.92 | 14.92 | 5 | 5.0 |
| Dendrobatidae | Hyloxalinae | Hyloxalus sp. Agua Azul | undefended | 1 | 14.30 | 14.30 | 8 | 8.0 |
| Dendrobatidae | Hyloxalinae | Hyloxalus toachi | undefended | 2 | 0.00–0.00 | 0.00 | 0–0 | 0.0 |
| Dendrobatidae | Dendrobatinae | Phyllobates aurotaenia | defended | 4 | 17.72–21.08 | 18.88 | 48–118 | 67.5 |
| Dendrobatidae | Dendrobatinae | Dendrobates truncatus | defended | 3 | 20.05–23.95 | 20.42 | 111–172 | 115.0 |
| Dendrobatidae | Dendrobatinae | Oophaga sylvatica | defended | 5 | 22.86–24.85 | 23.76 | 152–189 | 175.0 |
| Dendrobatidae | Dendrobatinae | Andinobates fulguritus | defended | 2 | 20.09–20.51 | 20.30 | 80–85 | 82.5 |
| Dendrobatidae | Dendrobatinae | Andinobates minutus | defended | 4 | 16.57–18.77 | 18.07 | 34–80 | 66.0 |
| Bufonidae | Amazophrynella siona | NA | 2 | 14.12–14.40 | 14.26 | 1–1 | 1.0 | |
| Bufonidae | Atelopus aff. spurrelli | NA | 1 | 11.58 | 11.58 | 4 | 4.0 | |
| Eleutherodactylidae | Eleutherodactylus cystignathoides* | NA | 3 | NA | NA | 0–0 | 0.0 | |
| Leptodactylidae | Leptodactylinae | Lithodytes lineatus | NA | 2 | 0.00–0.00 | 0.00 | 0–0 | 0.0 |
Additional files
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Supplementary file 1
Stomach content data for every individual.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp1-v1.xlsx
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Supplementary file 2
A summary of data available on alkaloid detection in undefended lineages of poison frogs.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp2-v1.docx
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Supplementary file 3
Collection localities, specimen numbers, size, sex, and summary of alkaloid quantities and diversity for each individual.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp3-v1.docx
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Supplementary file 4
Alkaloid-level data for every individual analyzed by GC-MS.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp4-v1.csv
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Supplementary file 5
S5a A feature table including information on Silverstoneia flotator and Eleutherodactylus cystignathoides skin alkaloids; S5b identifying information for samples corresponding to run numbers listed in Table S5a columns.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp5-v1.xlsx
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Supplementary file 6
List of the subset of classes and most specific classes of compounds in Silverstoneia flotator annotated as alkaloids (“Alkaloid Pathway” of NPClassifier) at >99% probability, their presence/absence in Eleutherodactylus cystignathoides, whether the compound is from one of the classes of lipophilic alkaloids listed in the Daly database, and whether the molecular formula for the metabolite is found in the Daly database.
- https://cdn.elifesciences.org/articles/100011/elife-100011-supp6-v1.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/100011/elife-100011-mdarchecklist1-v1.docx
