The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci USA

Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans Knoell Strasse 8, 07745 Jena, Germany.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 01/2008; 104(51):20427-31. DOI: 10.1073/pnas.0706229104
Source: PubMed


Ehrlich and Raven formally introduced the concept of stepwise coevolution using butterfly and angiosperm interactions in an attempt to account for the impressive biological diversity of these groups. However, many biologists currently envision butterflies evolving 50 to 30 million years (Myr) after the major angiosperm radiation and thus reject coevolutionary origins of butterfly biodiversity. The unresolved central tenet of Ehrlich and Raven's theory is that evolution of plant chemical defenses is followed closely by biochemical adaptation in insect herbivores, and that newly evolved detoxification mechanisms result in adaptive radiation of herbivore lineages. Using one of their original butterfly-host plant systems, the Pieridae, we identify a pierid glucosinolate detoxification mechanism, nitrile-specifier protein (NSP), as a key innovation. Larval NSP activity matches the distribution of glucosinolate in their host plants. Moreover, by using five different temporal estimates, NSP seems to have evolved shortly after the evolution of the host plant group (Brassicales) ( approximately 10 Myr). An adaptive radiation of these glucosinolate-feeding Pierinae followed, resulting in significantly elevated species numbers compared with related clades. Mechanistic understanding in its proper historical context documents more ancient and dynamic plant-insect interactions than previously envisioned. Moreover, these mechanistic insights provide the tools for detailed molecular studies of coevolution from both the plant and insect perspectives.

Download full-text


Available from: Heiko Vogel,
  • Source
    • " , Santalaceae , and Loranthaceae , and among members of the other three subfamilies of the Pieridae there are many tropical lineages ( DeVries , 2001 ) . This coincides with the fact that the estimated stem age of the Pieridae family is between 82 . 5 and 111 mya and the early evolution of tropical Brassicales is in the same temporal dimensions ( Wheat et al . , 2007 ; Beilstein et al . , 2010 ; Edger et al . , 2015 ) ."
    [Show abstract] [Hide abstract]
    ABSTRACT: The Brassicaceae include several major crop plants and numerous important model species in comparative evolutionary research such as Arabidopsis, Brassica, Boechera, Thellungiella, and Arabis species. As any evolutionary hypothesis needs to be placed in a temporal context, reliably dated major splits within the evolution of Brassicaceae are essential. We present a comprehensive time-calibrated framework with important divergence time estimates based on whole-chloroplast sequence data for 29 Brassicaceae species. Diversification of the Brassicaceae crown group started at the Eocene-to-Oligocene transition. Subsequent major evolutionary splits are dated to ∼20 million years ago, coinciding with the Oligocene-to-Miocene transition, with increasing drought and aridity and transient glaciation events. The age of the Arabidopsis thaliana crown group is 6 million years ago, at the Miocene and Pliocene border. The overall species richness of the family is well explained by high levels of neopolyploidy (43% in total), but this trend is neither directly associated with an increase in genome size nor is there a general lineage-specific constraint. Our results highlight polyploidization as an important source for generating new evolutionary lineages adapted to changing environments. We conclude that species radiation, paralleled by high levels of neopolyploidization, follows genome size decrease, stabilization, and genetic diploidization.
    The Plant Cell 09/2015; DOI:10.1105/tpc.15.00482 · 9.34 Impact Factor
    • "Recent molecular phylogenetic studies have shown significant increases in the diversification rate associated with parasitoid host shifts (Fordyce, 2010; McKenna and Farrell, 2006; McLeish et al., 2007; Wheat et al., 2007; Winkler et al., 2009). Host switching in insect parasitoids can have various ramifications . "
    [Show abstract] [Hide abstract]
    ABSTRACT: Pompilinae is one of the largest subfamilies of spider wasps (Pompilidae). Most pompilines are generalist spider predators at the family level, but some taxa exhibit ecological specificity (i.e., to spider-host guild). Here we present the first molecular phylogenetic analysis of Pompilinae, towards the aim of evaluating the monophyly of tribes and genera. We further test whether changes in the rate of diversification are associated with host-guild shifts. Molecular data were collected from five nuclear loci (28S, EF1-F2, LWRh, Wg, Pol2) for 76 taxa in 39 genera. Data were analyzed using maximum likelihood (ML) and Bayesian inference (BI). The phylogenetic results were compared with previous hypotheses of subfamilial and tribal classification, as well as generic relationships in the subfamily. The classification of Pompilus and Agenioideus is also discussed. A Bayesian relaxed molecular clock analysis was used to examine divergence times. Diversification rate-shift tests accounted for taxon-sampling bias using ML and BI approaches. Ancestral host family and host guild were reconstructed using MP and ML methods. Ancestral host guild for all Pompilinae, for the ancestor at the node where a diversification rate-shift was detected, and two more nodes back in time was inferred using BI. In the resulting phylogenies, Aporini was the only previously proposed monophyletic tribe. Several genera (e.g., Pompilus, Microphadnus and Schistonyx) are also not monophyletic. Dating analyses produced a well-supported chronogram consistent with topologies from BI and ML results. The BI ancestral host-use reconstruction inferred the use of spiders belonging to the guild "other hunters" (frequenting the ground and vegetation) as the ancestral state for Pompilinae. This guild had the highest probability for the ML reconstruction and was equivocal for the MP reconstruction; various switching events to other guilds occurred throughout the evolution of the group. The diversification of Pompilinae shows one main rate-shift coinciding with a shift to ground-hunter spiders, as reconstructed by the BI ancestral character-state analysis. Copyright © 2015. Published by Elsevier Inc.
    Molecular Phylogenetics and Evolution 08/2015; DOI:10.1016/j.ympev.2015.08.014 · 3.92 Impact Factor
  • Source
    • "The results of our correlation tests (Figs 1 and 2) show that both coccid species and coccid clade diversity (species richness within genera) are positively correlated with their host-plant family diversity. These findings are consistent with that found for other phytophagous insects, in which positive correlations with host plant clade richness have also been found (Farrell, 1998; Cuevas-Reyes et al., 2004; Janz et al., 2006; Wheat et al., 2007; Winkler & Mitter, 2008; Yoder & Nuismer, 2010; Janz, 2011). Interestingly, we found significant correlations between species richness and clade richness of both monophagous and polyphagous coccids with host-plant species richness. "
    [Show abstract] [Hide abstract]
    ABSTRACT: 1. The megadiverse herbivores and their host plants are a major component of biodiversity, and their interactions have been hypothesised to drive the diversification of both.2. If plant diversity influences the diversity of insects, there is an expectation that insect species richness will be strongly correlated with host-plant species richness. This should be observable at two levels (i) more diverse host-plant groups should harbour more species of insects, and (ii) the species richness of a group of insects should correlate with the richness of the host groups it uses. However, such a correlation is also consistent with a hypothesis of random host use, in which insects encounter and use hosts in proportion to the diversity of host plants. Neither of these expectations has been widely tested.3. These expectations were tested using data from a species-rich group of insects – the Coccidae (Hemiptera).4. Significant positive correlations were found between the species richness of coccid clades (genera) and the species richness of the host-plant family or families upon which the clades occur. On a global scale, more closely related plant families have more similar communities of coccid genera but the correlation is weak.5. Random host use could not be rejected for many coccids but randomisation tests and similarity of coccid communities on closely related plant families show that there is non-random host use in some taxa. Overall, our results support the idea that plant diversity is a driver of species richness of herbivorous insects, probably via escape-and-radiate or oscillation-type processes.
    Ecological Entomology 03/2015; 40(3). DOI:10.1111/een.12191 · 1.70 Impact Factor
Show more