Biozentrum Grindel

Hamburg, Germany

Biozentrum Grindel

Hamburg, Germany
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Petschenka G.,Biozentrum Grindel | Fandrich S.,Biozentrum Grindel | Sander N.,Biozentrum Grindel | Wagschal V.,Biozentrum Grindel | And 2 more authors.
Evolution | Year: 2013

Despite the monarch butterfly (Danaus plexippus) being famous for its adaptations to the defensive traits of its milkweed host plants, little is known about the macroevolution of these traits. Unlike most other animal species, monarchs are largely insensitive to cardenolides, because their target site, the sodium pump (Na+/K+-ATPase), has evolved amino acid substitutions that reduce cardenolide binding (so-called target site insensitivity, TSI). Because many, but not all, species of milkweed butterflies (Danaini) are associated with cardenolide-containing host plants, we analyzed 16 species, representing all phylogenetic lineages of milkweed butterflies, for the occurrence of TSI by sequence analyses of the Na+/K+-ATPase gene and by enzymatic assays with extracted Na+/K+-ATPase. Here we report that sensitivity to cardenolides was reduced in a stepwise manner during the macroevolution of milkweed butterflies. Strikingly, not all Danaini typically consuming cardenolides showed TSI, but rather TSI was more strongly associated with sequestration of toxic cardenolides. Thus, the interplay between bottom-up selection by plant compounds and top-down selection by natural enemies can explain the evolutionary sequence of adaptations to these toxins. © 2013 The Society for the Study of Evolution.


Bramer C.,Biozentrum Grindel | Dobler S.,Biozentrum Grindel | Deckert J.,Leibniz Institute For Evolutions Und Biodiversitatsforschung | Stemmer M.,Am Stux | And 2 more authors.
Proceedings of the Royal Society B: Biological Sciences | Year: 2015

Despite sequestration of toxins being a common coevolutionary response to plant defence in phytophagous insects, the macroevolution of the traits involved is largely unaddressed. Using a phylogenetic approach comprising species from four continents, we analysed the ability to sequester toxic cardenolides in the hemipteran subfamily Lygaeinae, which is widely associated with cardenolide-producing Apocynaceae. In addition, we analysed cardenolide resistance of their Na+/K+-ATPases, the molecular target of cardenolides. Our data indicate that cardenolide sequestration and cardenolide-resistant Na+/K+-ATPase are basal adaptations in the Lygaeinae. In two species that shifted to non-apocynaceous hosts, the ability to sequester was secondarily reduced, yet Na+/K+-ATPase resistance was maintained. We suggest that both traits evolved together and represent major coevolutionary adaptations responsible for the evolutionary success of lygaeine bugs. Moreover, specialization on cardenolides was not an evolutionary dead end, but enabled this insect lineage to host shift to cardenolide-producing plants from distantly related families. © 2015 The Author(s) Published by the Royal Society. All rights reserved.


Agrawal A.A.,Cornell University | Petschenka G.,Biozentrum Grindel | Bingham R.A.,Colorado College | Weber M.G.,Cornell University | Rasmann S.,University of Lausanne
New Phytologist | Year: 2012

Contents: Summary 28 I. Historic background and introduction 29 II. Diversity of cardenolide forms 29 III. Biosynthesis 30 IV. Cardenolide variation among plant parts 31 V. Phylogenetic distribution of cardenolides 32 VI. Geographic distribution of cardenolides 34 VII. Ecological genetics of cardenolide production 34 VIII. Environmental regulation of cardenolide production 34 IX. Biotic induction of cardenolides 36 X. Mode of action and toxicity of cardenolides 38 XI. Direct and indirect effects of cardenolides on specialist and generalist insect herbivores 39 XII. Cardenolides and insect oviposition 39 XIII. Target site insensitivity 40 XIV. Alternative mechanisms of cardenolide resistance 40 XV. Cardenolide sequestration 41 Acknowledgements 42 References 42 Summary: Cardenolides are remarkable steroidal toxins that have become model systems, critical in the development of theories for chemical ecology and coevolution. Because cardenolides inhibit the ubiquitous and essential animal enzyme Na +/K +-ATPase, most insects that feed on cardenolide-containing plants are highly specialized. With a huge diversity of chemical forms, these secondary metabolites are sporadically distributed across 12 botanical families, but dominate the Apocynaceae where they are found in >30 genera. Studies over the past decade have demonstrated patterns in the distribution of cardenolides among plant organs, including all tissue types, and across broad geographic gradients within and across species. Cardenolide production has a genetic basis and is subject to natural selection by herbivores. In addition, there is strong evidence for phenotypic plasticity, with the biotic and abiotic environment predictably impacting cardenolide production. Mounting evidence indicates a high degree of specificity in herbivore-induced cardenolides in Asclepias. While herbivores of cardenolide-containing plants often sequester the toxins, are aposematic, and possess several physiological adaptations (including target site insensitivity), there is strong evidence that these specialists are nonetheless negatively impacted by cardenolides. While reviewing both the mechanisms and evolutionary ecology of cardenolide-mediated interactions, we advance novel hypotheses and suggest directions for future work. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.


PubMed | Am Stux, Biozentrum Grindel, Leibniz Institute For Evolutions Und Biodiversitatsforschung and Cornell University
Type: Journal Article | Journal: Proceedings. Biological sciences | Year: 2015

Despite sequestration of toxins being a common coevolutionary response to plant defence in phytophagous insects, the macroevolution of the traits involved is largely unaddressed. Using a phylogenetic approach comprising species from four continents, we analysed the ability to sequester toxic cardenolides in the hemipteran subfamily Lygaeinae, which is widely associated with cardenolide-producing Apocynaceae. In addition, we analysed cardenolide resistance of their Na(+)/K(+)-ATPases, the molecular target of cardenolides. Our data indicate that cardenolide sequestration and cardenolide-resistant Na(+)/K(+)-ATPase are basal adaptations in the Lygaeinae. In two species that shifted to non-apocynaceous hosts, the ability to sequester was secondarily reduced, yet Na(+)/K(+)-ATPase resistance was maintained. We suggest that both traits evolved together and represent major coevolutionary adaptations responsible for the evolutionary success of lygaeine bugs. Moreover, specialization on cardenolides was not an evolutionary dead end, but enabled this insect lineage to host shift to cardenolide-producing plants from distantly related families.


Pankoke H.,Biozentrum Grindel | Bowers M.D.,University of Colorado at Boulder | Dobler S.,Biozentrum Grindel
Insect Biochemistry and Molecular Biology | Year: 2012

Herbivores with polyphagous feeding habits must cope with a diet that varies in quality. One of the most important sources of this variation in host plant suitability is plant secondary chemistry. We examined how feeding on plants containing one such group of compounds, the iridoid glycosides, might affect the growth and enzymatic activity in a polyphagous caterpillar that feeds on over 80 plant species in 50 different families. Larvae of the polyphagous arctiid, Grammia incorrupta, were reared exclusively on one of two plant species, one of which contains iridoid glycosides (Plantago lanceolata, Plantaginaceae) while the other does not (Taraxacum officinale, Asteraceae). Larval weight was measured on the two host plants, and midgut homogenates of last instar larvae were then assayed for activity and kinetic properties of β-glucosidases, using both a standard substrate, 4-nitrophenyl-β- d-glucose (NPβGlc), and the iridoid glycoside aucubin, one of the two main iridoid glycosides in P. lanceolata. Larvae feeding on P. lanceolata weighed significantly less and developed more slowly compared to larvae on T. officinale. While the larval midgut β-glucosidase activity determined with NPβGlc was significantly decreased when fed on P. lanceolata, aucubin was substantially hydrolyzed and the larval β-glucosidase activity towards both substrates correlated negatively with larval weight. Our results demonstrate that host plants containing high concentrations of iridoid glycosides have a negative impact on larval development of this generalist insect herbivore. This is most likely due to the hydrolysis of plant glycosides in the larval midgut which results in the release of toxic aglycones. Linking the reduced larval weight to the toxin-releasing action of an iridoid glycoside cleaving β-glucosidase, our results thus support the detoxification limitation hypothesis, suggesting fitness costs for the larvae feeding solely on P. lanceolata. Thus, in addition to the adaptive regulation of midgut β-glucosidase activity, host plant switching as a behavioral adaptation might be a prerequisite for generalist herbivores that allows them to circumvent the negative effects of plant secondary compounds. © 2012 Elsevier Ltd.


Petschenka G.,Biozentrum Grindel | Bramer C.,Biozentrum Grindel | Pankoke H.,Biozentrum Grindel | Dobler S.,Biozentrum Grindel
Basic and Applied Ecology | Year: 2011

Sequestration of toxic plant compounds by herbivorous insects as a defence against predators has been observed in many tritrophic systems. In this study, we focused on the potential benefit of sequestered cardenolides, potent toxins that block the Na+K+-ATPase against an invertebrate predator. To evaluate the effect of cardenolides we used three different types of cardenolide-containing prey, which were offered to the orb-weaving spider Nephila senegalensis. As a natural system spiders were presented with the cardenolide-sequestering moth Empyreuma pugione. To reduce the complexity of the predator-prey interaction spiders were furthermore fed with ouabain-laced non-toxic flies. Lastly, we developed a new reductionistic assay involving gelatine capsules as insect dummies. Our results show that ouabain elicits significant rejection behaviour and suggest cardenolides to be the basis for rejection of E. pugione by N. senegalensis. © 2011 Gesellschaft für Ökologie.


Two known and two new species, as well as two new genera from the deep sea of the south-western Atlantic, Cape Basin and the Weddell Sea are described, including Leptostyloides secundus n. sp. and Pseudoleptostyloides mediosetosus n. gen. and n. sp. The diagnosis of the genera Divacuma and Leptostyloides are improved, the species Makrokylindrus paradivacumatus is transferred to the new genus Austrostylis, and the species Leptostyoides longiappendiculata is transferred to Pseudoleptostyloides n. gen. © 2014, Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg.


Haas A.,Biozentrum Grindel | Das I.,University Malaysia Sarawak
Bonner Zoologische Monographien | Year: 2011

Our ad hoc survey of 130 books and monographs showed that almost 70% did not present any descriptive information on larval anurans, and when larval stages were included the quality of documentation often tended to be poor. The larval (or developmental) stages of 51 species of east Malaysian frogs still remain unknown. Modern methods and techniques have changed the way we treat larvae taxonomically, and we recommend their adoption in tadpole research. Notably, DNA barcoding allows for unequivocal matching with adult frogs, and digital color photography provides documentation of tadpole features of unprecedented quality, partly replacing traditional drawings. Both techniques are considered essential for the study of tadpoles. Tadpole measurements have now reached a high level of standardization and can be performed quickly, accurately, and easily with digital microscopes. Nevertheless, line drawings and SEM may still be valuable techniques when certain details need to be demonstrated.


Natalia A.,University of Buenos Aires | Muhlenhardt-Siegel U.,Biozentrum Grindel
Zootaxa | Year: 2010

Two new deep-sea cumaceans, Diastylis andeepae and D. catalinae are described from the Weddell Sea. Diastylis andeepae n. sp. can be distinguished from other members of the genus by a combination of characters including: carapace with small tubercles all over and anterior part with an arched row of teeth extending from each side of the pseudorostrum and disappearing a short distance before reaching the inferior margin of the carapace, ischium of the pereopod 2 with four strong teeth, endopod uropod of two articles. Diastylis catalinae n. sp. is a closely related species to D. richardi Fage 1929 recorded from the Bay of Biscay, however D. catalinae can be easily separated from D. richardi by having: (1) on each side of the anterior part of the carapace several teeth arranged in two non-uniform rows (randomly distributed and with two antero-lateral horns in D. richardi); (2) clearly visible pereonites 1 and 2 in dorsal view (hardly visible in D. richardi); (3) one tooth on each postero-lateral angle of the pereonite 5 (without teeth in D.richardi); and (4) one minute simple seta on article 4 of the antenna 2 (a long setulate seta in D. richardi). Copyright © 2010 Magnolia Press.


Pankoke H.,Biozentrum Grindel | Bowers M.D.,University of Colorado at Boulder | Dobler S.,Biozentrum Grindel
Journal of Insect Physiology | Year: 2010

Iridoid glycosides are secondary plant compounds that have deterrent, growth reducing or even toxic effects on non-adapted herbivorous insects. To investigate the effects of iridoid glycoside containing plants on the digestive metabolism of a generalist herbivore, larvae of Spilosoma virginica (Lepidoptera: Arctiidae) were reared on three plant species that differ in their secondary plant chemistry: Taraxacum officinale (no iridoid glycosides), Plantago major (low iridoid glycoside content), and P. lanceolata (high iridoid glycoside content). Midguts of fifth instar larvae were assayed for the activity and kinetic properties of β-glucosidase using different substrates. Compared to the larvae on T. officinale, the β-glucosidase activity of larvae feeding on P. lanceolata was significantly lower measured with 4-nitrophenyl-β-. d-glucopyranoside. Using the iridoid glycoside aucubin as a substrate, we did not find differences in the β-glucosidase activity of the larvae reared on the three plants. Heat inactivation experiments revealed the existence of a heat-labile and a more heat-stable β-glucosidase with similar Michaelis constants for 4-nitrophenyl-β-. d-glucopyranoside. We discuss possible mechanisms leading to the observed decrease of β-glucosidase activity for larvae reared on P. lanceolata and its relevance for generalist herbivores in adapting to iridoid glycoside containing plant species and their use as potential host plants. © 2010 Elsevier Ltd.

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