The genetic basis of a plant-insect coevolutionary key innovation.

Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans Knoell Strasse 8, 07745 Jena, Germany.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 01/2008; 104(51):20427-31. DOI: 10.1073/pnas.0706229104
Source: PubMed

ABSTRACT 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.

  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Foreign plants are usually introduced for food or aesthetic reasons. Most of these plants are non-invasive, but can alter the evolutionary trajectory of the associated native insects or inadvertently spread potential pests. A hitherto poorly documented example is the rapid expansion of Chilades pandava, a Cycas-feeding butterfly. Since about 1990, large numbers of the Sago Palm Cycas revoluta were introduced into Taiwan. Invading or introduced with this hostplant, Ch. pandava has rapidly spread to all major parts of Taiwan and to other places worldwide. In order to trace the source of outbreaks, I set this issue as the first part of this dissertation (Part I). In part II, the members in the genus Chilades include some of the smallest butterflies in the world. As for some other small butterflies classified in the same lycaenid tribe, Polyommatini, they are widely distributed, ranging from West Africa to East Asia. Larval hostplant associations are unusually wide for a single butterfly genus, including both gymnosperms and angiosperms, questioning the monophyly of Chilades butterflies and the hostplant associations among this genus butterflies. In part I, total 810 specimens were sampled covering 50 Taiwanese localities and other regions using mitochondrial COII sequences. Only 29 haplotypes were found, however, the haplotype C which dominates outbreak populations from western Taiwan was endemic to the island. This is consistent with the hypothesis of a local range expansion of Ch. pandava, rather than an introduction. In addition, the Taiwanese Central Mountain Ridge may constitute a primary biogeographic barrier 6 restricting gene flow between eastern and western populations. In part II, to reconstruct the relationships of the genus Chilades and map patterns of hostplant use onto this inferred tree, mitochondrial COI, COII and nuclear EF-1α sequences (3437 bp, total 82 taxa) were used. The topologies show that Chilades is polyphyletic containing two separated clades, and that gymnosperm specialists (feeding on cycads) are monophyletic and represent a single host shift from angiosperms (Fabaceae). The study of tracing the source of outbreaks populations not only flags an important new invasive insect that needs to be monitored and controlled within the horticultural trade and for in situ cycad conservation, but also provides a clearly documented case of the transformation of a native tropical butterfly into a pest via introduced horticultural plants. In the aspect of genus status, once butterflies belonging to the genus Freyeria (which is usually treated as synonym of Chilades, but is here resurrected, including Freyeria putli, F. minuscula, F. trochylus, and F. yunnanensis comb. nov.) are excluded, the genus Chilades becomes monophyletic, but still comprising both angiosperm and gymnosperm (cycad) feeders. In this part, I infer the correct phylogenetic placement of both Chilades and Freyeria, African origins for Chilades, and also an aspect to reconstructing the genera relationships among Eliot’s Polyommatus section.
    01/2010, Degree: PhD, Supervisor: Yu-Feng Hsu
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The montane forests of Africa represent some of the Earth's most diverse and threatened ecosystems. In particular, those in West Africa have received comparatively little attention from scientists in terms of understanding the ecology and biodiversity of their species. This thesis wishes to understand genetic and ecological factors that underpin the long-term survival of selected tree species (Cordia millenii, Entandrophragma angolense, Lovoa trichilioides) in the montane forests of the Mambilla Plateau, Nigeria. The results obtained here provide a strong foundation for future work that wishes to preserve the diverse forests of this region.
    01/2014, Degree: MSc Evolutionary Biology, University of Canterbury, Supervisor: Senior supervisor: A/prof Hazel Chapamn, Associate supervisors: Dr Marie Hale & Daniel Stouffer
  • [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; DOI:10.1111/een.12191 · 1.97 Impact Factor

Full-text (2 Sources)

Available from
May 20, 2014