Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)
- University of Bern, Switzerland
- Boyce Thompson Institute, United States
- University of Missouri, United States
- Justus-Liebig-Universität, Germany
- Estación Experimental de Zonas Áridas, Spain
- Universidad de Granada, Spain
- Bielefeld University, Germany
Abstract
Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9,869 orthologous genes, revealing several geographic clades but also high levels gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.
Data availability
Sequence data are available under GenBank project ID PRJNA563696 and www.erysimum.org, while all trait data and R code for trait and phylogenetic analyses are available from the Dryad Digital Repository
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Data from: Rapid and independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)Dryad Digital Repository, doi:10.5061/dryad.7hb5c59.
Article and author information
Author details
Francisco Perfectti
Funding
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PZ00P3-161472)
- Tobias Züst
National Science Foundation (1811965)
- Cynthia K Holland
Triad Foundation
- Susan R Strickler
- Georg Jander
National Science Foundation (1645256)
- Georg Jander
Deutsche Forschungsgemeinschaft (DFG-PE 2059/3-1)
- Georg Petschenka
Agencia Estata de Investigacion, Spain (CGL2017-86626-C2-2-P)
- Francisco Perfectti
LOEWE Program Insect Biotechnology and Bioresources
- Georg Petschenka
Junta de Andalucia Programa Operativo (FEDER 2014-2020 A-RNM-505-UGR18)
- Francisco Perfectti
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2020, Züst et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)
eLife 9:e51712.
https://doi.org/10.7554/eLife.51712
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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.
