Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses
Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biase...
| Κύριοι συγγραφείς: | , , , , , , , , , , , , |
|---|---|
| Μορφή: | Άρθρο |
| Γλώσσα: | English |
| Έκδοση: |
eLife Sciences Publications Ltd
2024-12-01
|
| Σειρά: | eLife |
| Θέματα: | |
| Διαθέσιμο Online: | https://elifesciences.org/articles/100011 |
| _version_ | 1826918114381529088 |
|---|---|
| author | Rebecca D Tarvin Jeffrey L Coleman David A Donoso Mileidy Betancourth-Cundar Karem López-Hervas Kimberly S Gleason J Ryan Sanders Jacqueline M Smith Santiago R Ron Juan C Santos Brian E Sedio David C Cannatella Richard W Fitch |
| author_facet | Rebecca D Tarvin Jeffrey L Coleman David A Donoso Mileidy Betancourth-Cundar Karem López-Hervas Kimberly S Gleason J Ryan Sanders Jacqueline M Smith Santiago R Ron Juan C Santos Brian E Sedio David C Cannatella Richard W Fitch |
| author_sort | Rebecca D Tarvin |
| collection | DOAJ |
| description | Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins. |
| first_indexed | 2025-02-17T12:44:58Z |
| format | Article |
| id | doaj.art-901b61acb0b9449eaaaac32b078d4846 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2025-02-17T12:44:58Z |
| publishDate | 2024-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-901b61acb0b9449eaaaac32b078d48462024-12-27T14:10:19ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.100011Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defensesRebecca D Tarvin0https://orcid.org/0000-0001-5387-7250Jeffrey L Coleman1https://orcid.org/0000-0002-8156-5948David A Donoso2https://orcid.org/0000-0002-3408-1457Mileidy Betancourth-Cundar3https://orcid.org/0000-0003-2368-6028Karem López-Hervas4https://orcid.org/0000-0002-8296-377XKimberly S Gleason5J Ryan Sanders6Jacqueline M Smith7Santiago R Ron8Juan C Santos9Brian E Sedio10https://orcid.org/0000-0002-1723-9822David C Cannatella11Richard W Fitch12https://orcid.org/0000-0002-4927-725XMuseum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology and Biodiversity Collections, University of Texas at Austin, Austin, United States; Smithsonian Tropical Research Institute, Ancón, PanamaGrupo de Investigación en Ecología Evolutiva en los Trópicos (EETROP), Universidad de las Américas, Quito, Ecuador; Ecological Networks Lab, Technische Universität Darmstadt, Darmstadt, GermanyDepartamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia; Department of Biology, Stanford University, Palo Alto, United StatesMax Planck Institute for Evolutionary Biology, Plön, GermanyDepartment of Chemistry and Physics, Indiana State University, Terre Haute, United StatesDepartment of Chemistry and Physics, Indiana State University, Terre Haute, United StatesDepartment of Chemistry and Physics, Indiana State University, Terre Haute, United StatesMuseo de Zoología, Escuela de Biología, Facultad de Ciencias Exactas y Naturales, Pontificia Universidad Católica del Ecuador, Quito, EcuadorDepartment of Biological Sciences, St John’s University, New York, United StatesDepartment of Integrative Biology and Biodiversity Collections, University of Texas at Austin, Austin, United States; Smithsonian Tropical Research Institute, Ancón, PanamaDepartment of Integrative Biology and Biodiversity Collections, University of Texas at Austin, Austin, United StatesDepartment of Chemistry and Physics, Indiana State University, Terre Haute, United StatesUnderstanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.https://elifesciences.org/articles/100011toxin sequestrationtoxin resistancebioaccumulationnoveltyadaptive landscapetoxicokinetics |
| spellingShingle | Rebecca D Tarvin Jeffrey L Coleman David A Donoso Mileidy Betancourth-Cundar Karem López-Hervas Kimberly S Gleason J Ryan Sanders Jacqueline M Smith Santiago R Ron Juan C Santos Brian E Sedio David C Cannatella Richard W Fitch Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses eLife toxin sequestration toxin resistance bioaccumulation novelty adaptive landscape toxicokinetics |
| title | Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| title_full | Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| title_fullStr | Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| title_full_unstemmed | Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| title_short | Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| title_sort | passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses |
| topic | toxin sequestration toxin resistance bioaccumulation novelty adaptive landscape toxicokinetics |
| url | https://elifesciences.org/articles/100011 |
| work_keys_str_mv | AT rebeccadtarvin passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT jeffreylcoleman passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT davidadonoso passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT mileidybetancourthcundar passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT karemlopezhervas passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT kimberlysgleason passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT jryansanders passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT jacquelinemsmith passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT santiagorron passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT juancsantos passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT brianesedio passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT davidccannatella passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses AT richardwfitch passiveaccumulationofalkaloidsininconspicuouslycoloredfrogsrefinestheevolutionaryparadigmofacquiredchemicaldefenses |