The adaptive significance of insect gall morphology
TL;DR: It is suggested that the hypothesis that selection imposed by enemies remains the most probable adaptive explanation for the evolution of diversity in insect galls has yet to be tested explicitly, and the requirements for an appropriate cross-species analysis are discussed.
Abstract: Insect galls are dramatic examples of extended phenotypes: although composed of host plant tissues, their development is largely controlled by insect genes. Adaptive explanations for gall traits should thus be expressed in terms of impacts on insect fitness, but the extent to which interspecific variation in gall structure is adaptive, and the possible selective pressures driving diversification in gall form remain controversial. In colonial aphids and thrips, gall structures probably diversified in response to selection for enhancement of the surface area available for feeding. In other taxa, such as gall wasps and gall midges, diversity is expressed predominantly in non-nutritive tissues, particularly those on the gall surface. All natural enemies attack the occupants of closed galls by penetrating gall tissue, and modifications that reduce enemy attack rates should thus be favoured. Recent studies of intraspecific variation in gall form strongly support a defensive role for several traits, but, to date, there is little empirical support for enemies as a cause of interspecific variation in gall form. Selection imposed by enemies nevertheless remains the most probable adaptive explanation for the evolution of diversity. We suggest that this hypothesis has yet to be tested explicitly, and discuss the requirements for an appropriate cross-species analysis.
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TL;DR: Extensive qualitative and quantitative high throughput analyses of temporal and spatial variations in gene expression, protein level and activity, and metabolite concentration will accelerate not only the understanding of the overall mechanisms of direct defense, but also accelerate the identification of specific targets for enhancement of plant resistance for agriculture.
Abstract: Plants respond to insect herbivory with responses broadly known as direct defenses, indirect defenses, and tolerance. Direct defenses include all plant traits that affect susceptibility of host plants by themselves. Overall categories of direct plant defenses against insect herbivores include limiting food supply, reducing nutrient value, reducing preference, disrupting physical structures, and inhibiting chemical pathways of the attacking insect. Major known defense chemicals include plant secondary metabolites, protein inhibitors of insect digestive enzymes, proteases, lectins, amino acid deaminases and oxidases. Multiple factors with additive or even synergistic impact are usually involved in defense against a specific insect species, and factors of major importance to one insect species may only be of secondary importance or not effective at all against another insect species. Extensive qualitative and quantitative high throughput analyses of temporal and spatial variations in gene expression, protein level and activity, and metabolite concentration will accelerate not only the understanding of the overall mechanisms of direct defense, but also accelerate the identification of specific targets for enhancement of plant resistance for agriculture.
384 citations
Cites background from "The adaptive significance of insect..."
...In this zone (gall), the insect experiences a selective advantage because of enhanced nutrition (due to the formation of a nutrient sink) and reduced plant defense (Stone & Schönrogge, 2003; Harris et al., 2006; Zhu et al., 2007)....
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TL;DR: Herbivores have evolved diverse strategies to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring, and the ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms.
234 citations
Additional excerpts
...…Jonckheere, W.; Knegt, B.; Lemos, F.; Liu, J.; Schimmel, B.C.J.; Villarroel, C.A.; Ataide, L.M.S.; Dermauw, W.; Glas, J.J.; Egas, M.; Janssen, A.; Van Leeuwen, T.; Schuurink, R.C.; Sabelis, M.W.; Alba, J.M. DOI 10.1093/aob/mcv054 Publication date 2015 Document Version Accepted author manuscript...
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TL;DR: D.J. Shorthouse, A. Raman, and D.D. Wool are among the artists whose work has been exhibited at the Whitney Museum of American Art in New York City this year.
215 citations
TL;DR: This paper proposed a tri-trophic niche concept for phytophagous insects to reconcile ecological and evolutionary approaches through the concept of the ecological niche, arguing that these niche concepts have different implications for understanding herbivore community structure, population divergence, and evolutionary diversification.
Abstract: A conceptual divide exists between ecological and evolutionary approaches to understanding adaptive radiation, although the phenomenon is inherently both ecological and evolutionary. This divide is evident in studies of phytophagous insects, a highly diverse group that has been frequently investigated with the implicit or explicit goal of understanding its diversity. Whereas ecological studies of phytophagous insects increasingly recognize the importance of tri-trophic interactions as determinants of niche dimensions such as host-plant associations, evolutionary studies typically neglect the third trophic level. Here we attempt to reconcile ecological and evolutionary approaches through the concept of the ecological niche. We specifically present a tri-trophic niche concept as a foil to the traditional bi-trophic niche concept for phytophagous insects. We argue that these niche concepts have different implications for understanding herbivore community structure, population divergence, and evolutionary diversification. To this end, we offer contrasting empirical predictions of bi- and tri-trophic niche concepts for patterns of community structure, the process of population divergence, and patterns of evolutionary diversification of phytophagous insects.
193 citations
TL;DR: It is shown that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts, most likely Wolbachia, to manipulate the physiology of its host plant resulting in the ‘green-island’ phenotype—photosynthetically active green patches in otherwise senescent leaves—and to increase its fitness.
Abstract: The life cycles of many organisms are constrained by the seasonality of resources. This is particularly true for leaf-mining herbivorous insects that use deciduous leaves to fuel growth and reproduction even beyond leaf fall. Our results suggest that an intimate association with bacterial endosymbionts might be their way of coping with nutritional constraints to ensure successful development in an otherwise senescent environment. We show that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts, most likely Wolbachia, to manipulate the physiology of its host plant resulting in the ‘green-island’ phenotype—photosynthetically active green patches in otherwise senescent leaves—and to increase its fitness. Curing leaf-miners of their symbiotic partner resulted in the absence of green-island formation on leaves, increased compensatory larval feeding and higher insect mortality. Our results suggest that bacteria impact green-island induction through manipulation of cytokinin levels. This is the first time, to our knowledge, that insect bacterial endosymbionts have been associated with plant physiology.
190 citations
Cites background from "The adaptive significance of insect..."
...However, the molecules and mechanisms involved in insect gall formation remain totally unknown (Stone et al. 2002; Stone & Schönrogge 2003). r for correspondence (david.giron@univ-tours.fr). ic supplementary material is available at http://dx.doi.org/10. b.2010.0214 or via…...
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References
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TL;DR: This review summarizes the current knowledge on the biosynthesis, structure, and function of this new class of signaling molecules and discusses the possibility that these signals could be part of a new family of plant lipo-chitooligosaccharide growth regulators.
Abstract: Rhizobia elicit on their specific leguminous hosts the formation of new organs, called nodules, in which they fix nitrogen. The rhizobia] nodulation genes specify the synthesis of lipo-chitooligosaccharide signals, the Nod factors (NFs). Each rhizobial species has a characteristic set of nodulation genes that specifies the length of the chitooligosaccharide backbone and the type of substitutions at both ends of the molecule, thus making the NFs specific for a given plant host. At extremely low concentrations, purified NFs are capable of eliciting on homologous legume hosts many of the plant developmental responses characteristic of the bacteria themselves, including cell divisions, and the triggering of a plant organogenic program. This review summarizes our current knowledge on the biosynthesis, structure, and function of this new class of signaling molecules. Finally we discuss the possibility that these signals could be part of a new family of plant lipochitooligosaccharide growth regulators.
925 citations
TL;DR: The evolution of the galling habit has followed two pathways, one via mining plant tissues and the other from sedentary external herbivores that then modify plant growth.
Abstract: Major hypotheses on the adaptive significance of insect gall formation are reviewed: nonadaptive, plant protection, mutual benefit, nutrition, microenvironment, and enemy hypotheses. We evaluate the validity of each, and find the first three to be without merit because galls clearly have adaptive features for the insect, but few if any for the plant, and the galler has negative impact on the plant, making the relationship parasitic. Predictions are developed to enable testing of hypotheses, and tests are discussed. Nutrition and microenvironment hypotheses are supported, while the enemy hypothesis remains with several uncertain issues to be resolved. The evolution of the galling habit has followed two pathways, one via mining plant tissues and the other from sedentary external herbivores that then modify plant growth. In each route the sequence of selective factors was probably different, but improved protection from hygrothermal stress and improved nutrition are of primary importance, and protection from enemies probably reinforced the galling habit.
514 citations
TL;DR: This work assesses the importance of gall traits in structuring oak cynipid communities and summarize the evidence for bottom-up and top-down effects across trophic levels, and identifies major unanswered questions and suggest approaches for the future.
Abstract: Oak gall wasps (Hymenoptera: Cynipidae, Cynipini) are characterized by possession of complex cyclically parthenogenetic life cycles and the ability to induce a wide diversity of highly complex species- and generation-specific galls on oaks and other Fagaceae. The galls support species-rich, closed communities of inquilines and parasitoids that have become a model system in community ecology. We review recent advances in the ecology of oak cynipids, with particular emphasis on life cycle characteristics and the dynamics of the interactions between host plants, gall wasps, and natural enemies. We assess the importance of gall traits in structuring oak cynipid communities and summarize the evidence for bottom-up and top-down effects across trophic levels. We identify major unanswered questions and suggest approaches for the future.
447 citations
TL;DR: It is confirmed that current coevolutionary selection in interspecific interactions can be highly divergent across both narrow and broad geographic scales, thereby fuelling continuing coev evolution of taxa.
Abstract: Coevolution of species is one of the major processes organizing the Earth's biodiversity. Recent coevolutionary theory has indicated that the geographic structure of species has the potential to impose powerful and continuing effects on coevolutionary dynamics, if that structure creates selection mosaics and coevolutionary hotspots across landscapes. Here we confirm that current coevolutionary selection in interspecific interactions can be highly divergent across both narrow and broad geographic scales, thereby fueling continuing coevolution of taxa. Study of a widespread plant insect interaction across a broad range of habitats for several years showed that an insect functioning both as a pollinator and a floral parasite can be strongly mutualistic in some habitats but commensal or antagonistic in neighbouring habitats. The results for one of the habitats span seven years, demonstrating that the local structure of coevolutionary selection can remain stable across multiple generations. Conservation of the evolutionary processes maintaining long-term biological diversity may require preservation of the conditions that allow a long-term shifting geographic mosaic of coevolutionary hotspots and coldspots.
439 citations