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Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore.

Herbivory induces both direct and indirect defenses in plants; however, some combinations of these defenses may not be compatible. The jasmonate signal cascade activated both direct (nicotine accumulations) and indirect (mono- and sesquiterpene emissions) whole-plant defense responses in the native tobacco Nicotiana attenuata Torr. Ex Wats. Nicotine accumulations were proportional to the amount of leaf wounding and the resulting increases in jasmonic acid (JA) concentrations. However, when larvae of the nicotine-tolerant herbivore, Manduca sexta, fed on plants or their oral secretions were applied to leaf punctures, the normal wound response was dramatically altered, as evidenced by large (4- to 10-fold) increases in the release of (i) volatile terpenoids and (ii) ethylene, (iii) increased (4- to 30-fold) accumulations of endogenous JA pools, but (iv) decreased or unchanged nicotine accumulations. The ethylene release, which was insensitive to inhibitors of induced JA accumulation, was sufficient to account for the attenuated nicotine response. Applications of ethylene and ethephon suppressed the induced nicotine response and pre-treatment of plants with a competitive inhibitor of ethylene receptors, 1-methylcyclopropene, restored the full nicotine response. This ethylene burst, however, did not inhibit the release of volatile terpenoids. Because parasitoids of Manduca larvae are sensitive to the dietary intake of nicotine by their hosts, this ethylene-mediated switching from direct to a putative indirect defense may represent an adaptive tailoring of a plant's defense response.

Acetates↗

Cucurbitacins in Plant-Insect Interactions: Biosynthesis, Regulation, Ecological Functions, and Prospects for Crop Protection.

Cucurbitacins are highly oxygenated tetracyclic triterpenoids characterized by intense bitterness, substantial structural diversity, and important consequences for plant-herbivore interactions. Although best known from Cucurbitaceae, cucurbitacins and related cucurbitane-type metabolites also occur in phylogenetically distant herbaceous and woody plants. Genetic and biochemical studies have validated several core biosynthetic steps, including cucurbitadienol formation by oxidosqualene cyclases and subsequent modification by cytochrome P450 monooxygenases, acyltransferases, and glycosyltransferases. Tissue-preferential basic helix-loop-helix transcription factors constitute the best-characterized regulatory layer, whereas the evidence supporting accessory regulators, transporters, and environmental responses varies from functional validation to transcriptomic or genomic prediction. From the plant perspective, cucurbitacins deter feeding or impair performance in many generalist and non-adapted herbivores. By contrast, their use as host-recognition cues and feeding stimulants by specialist diabroticite beetles reflects evolved herbivore adaptations involving perception, tolerance, metabolism, or sequestration rather than a second defensive function of the plant trait. Herbivore-induced cucurbitacin accumulation has been demonstrated in particular systems, although its regulatory mechanisms and ecological generality remain unresolved. Unlike previous reviews centered primarily on cucurbitacin chemistry, pharmacological activity, or individual biosynthetic pathways, this review integrates evidence-graded pathway reconstruction and molecular regulation with taxonomic distribution, insect adaptation, domestication, and agroecological consequences. Mechanistically, this review traces how scaffold formation, oxidative tailoring, conjugation, tissue-specific regulation, and transport give rise to contrasting ecological outcomes through herbivore-specific perception, tolerance, metabolism, and sequestration. We conclude that uniformly increasing or eliminating cucurbitacins is unlikely to provide broadly effective crop resistance because either direction may favor a different herbivore group. Future priorities include functional validation of candidate genes, spatially resolved metabolite analysis, comparative investigation of non-cucurbit lineages, and field evaluation involving generalist and specialist herbivores, crop quality, and non-target organisms. These advances will support context-specific fruit-quality improvement, behavioral pest control, and integrated pest management strategies rather than cucurbitacin manipulation as a stand-alone resistance approach.

agroecology↗

Molar tooth diversity, disparity, and ecology in Cenozoic ungulate radiations.

A classic example of adaptive radiation is the diversification of Cenozoic ungulates into herbivore adaptive zones. Their taxonomic diversification has been associated with changes in molar tooth morphology. Analysis of molar crown types of the Artiodactyla, Perissodactyla, and archaic ungulates ("Condylarthra") shows that the diversity of genera and crown types was high in the Eocene. Post-Eocene molars of intermediate crown types are rare, and thus the ungulate fauna contained more taxa having fewer but more disparate crown types. Taxonomic diversity trends alone give incomplete descriptions of adaptive radiations.

Animals↗

Nicotine's defensive function in nature.

Plants produce metabolites that directly decrease herbivore performance, and as a consequence, herbivores are selected for resistance to these metabolites. To determine whether these metabolites actually function as defenses requires measuring the performance of plants that are altered only in the production of a certain metabolite. To date, the defensive value of most plant resistance traits has not been demonstrated in nature. We transformed native tobacco(Nicotiana attenuata) with a consensus fragment of its two putrescine N-methyl transferase (pmt) genes in either antisense or inverted-repeat (IRpmt) orientations. Only the latter reduced (by greater than 95%) constitutive and inducible nicotine. With D(4)-nicotinic acid (NA), we demonstrate that silencing pmt inhibits nicotine production, while the excess NA dimerizes to form anatabine. Larvae of the nicotine-adapted herbivore Manduca sexta (tobacco hornworm) grew faster and, like the beetle Diabrotica undecimpunctata, preferred IRpmt plants in choice tests. When planted in their native habitat, IRpmt plants were attacked more frequently and, compared to wild-type plants, lost 3-fold more leaf area from a variety of native herbivores, of which the beet armyworm, Spodoptera exigua, and Trimerotropis spp. grasshoppers caused the most damage. These results provide strong evidence that nicotine functions as an efficient defense in nature and highlights the value of transgenic techniques for ecological research.

Animals↗

Fast track to the trichome: induction of N-acyl nornicotines precedes nicotine induction in Nicotiana repanda.

Nicotiana repanda Wildenow ex Lehmann acylates nornicotine in its trichomes to produce N-acyl-nornicotine (NacNN) alkaloids which are dramatically more toxic than nicotine is to the nicotine-adapted herbivore, Manduca sexta. These NacNNs, like nicotine, were induced by methyl jasmonate (MeJA) and wounding, but the 2-fold increase in NacNN pools was much faster (within 6 h) than the MeJA-induced increase in nornicotine pools (24 h to 4 d), its parent substrate. When 15NO(-)3 pulse-chase experiments with intact and induced plants were used to follow the incorporation of 15N into alkaloids in different plant parts over the plant's lifetime, it was found that the root nicotine pool was most rapidly labeled, followed by the shoot nornicotine and NacNN pools. After 3 d, 3.12% of 15N acquired was in nicotine (0.93%), nornicotine (0.32%) and NacNNs (1.73%) while only 0.14% was in anabasine. Once NacNNs are externalized to the leaf surface, they are not readily re-distributed within the plant and are lost with senescing leaves. The wound- and MeJA-induced N-acylation of nornicotine is independent of induced changes in nornicotine pools and the rapidity of the response suggests its importance in defense against herbivores.

Acetates↗

Variable diets and changing taste in plant-insect relationships.

The host ranges of phytophagous insects are determined to a large degree by plant chemistry. Specialist insects are often closely associated with plants that produce characteristic chemicals, which may act as attractants or stimulants to aid in finding or recognizing a host. Generalist insects are generally believed to rely on the presence of repellents or deterrents to ensure avoidance of unsuitable plants. However, the chemistry of any plant can be highly variable, as a result of growth characteristics, genetic variation, or environmental factors. Such variable chemistry may provide windows of opportunity for nonadapted insects to utilize a plant or for a plant to become resistant to a normally adapted herbivore. Differences in insect responses to plant constituents may also result from genetic variation or environmental factors. In particular, dietary experience has been found to influence the ability of insects to taste plant chemicals that may serve as signals of suitability or unsuitability. Certain dietary constituents appear to suppress the development of taste sensitivity to deterrents in an insect, whereas the presence of specific stimulants in the diet may result in the development of dependence on these compounds. These findings further emphasize the fact that the dynamics of plant biochemistry along with plasticity in the sensory system of insects might be expected to play a major role in the evolution of new plant-insect relationships.

Animals↗

The hypocone as a key innovation in mammalian evolution.

The hypocone, a cusp added to the primitively triangular upper molar teeth of therian mammals, has evolved convergently > 20 times among mammals during the Cenozoic. Acquisition of the hypocone itself involves little phenotypic change, but subsequent diversification of groups possessing the hypocone may be greatly enhanced. Our analysis of the Cenozoic mammalian radiations, including the Recent fauna, shows that high species diversity of mammals with hypocones and association of the hypocone with herbivory strongly support recognition of the hypocone as a key innovation that has allowed invasion of, and diversification within, herbivorous adaptive zones. In contrast, mammals lacking hypocones show no marked increase in species diversity during the Cenozoic.

Animals↗

Silencing the jasmonate cascade: induced plant defenses and insect populations.

We transformed the native tobacco, Nicotiana attenuata, to silence its lipoxygenase, hydroperoxide lyase, and allene oxide synthase genes in order to inhibit oxylipin signaling, known to mediate the plant's direct and indirect defenses. When planted into native habitats, lipoxygenase-deficient plants were more vulnerable to N. attenuata's adapted herbivores but also attracted novel herbivore species, which fed and reproduced successfully. In addition to highlighting the value of genetically silencing plants to study ecological interactions in nature, these results show that lipoxygenase-dependent signaling determines host selection for opportunistic herbivores and that induced defenses influence herbivore community composition.

Acetates↗

Host-plant adaptation in an herbivorous marine amphipod: genetic potential not realized in field populations.

Evolutionary responses of herbivores to their host plants depend not only on selection from plants, but also on the genetic basis of traits relating to host use. The genetic basis of such traits has been investigated extensively among terrestrial insect herbivores, but has received almost no attention among marine herbivores. We tested whether performance traits in the herbivorous marine amphipod Peramphithoe parmerong display heritable variation and, for the first time for a marine herbivore, whether selection has resulted in local adaptation to host plants on two spatial scales. Peramphithoe parmerong displayed heritable genetic variation for survival on two host macroalgae, the high-quality Sargassum linearifolium and the poor-quality Padina crassa, and for growth on S. linearifolium. Differences in performance on different hosts thus have the potential to select for differential use of hosts by this amphipod. Despite this potential, there was no evidence among field populations of local adaptation to host algae on either scale tested: between hosts within a site or among sites differing in algal species composition. Within a site, amphipods were not more likely to prefer or perform better on the host on which they were collected. Similarly, amphipods collected from sites in which P. crassa was present were not more likely to perform well on this host than amphipods collected from sites where this alga was not found. Ecological factors that may explain the persistence of P. parmerong on P. crassa and the possibility of phylogenetic constraints on host use by P. parmerong are discussed.

Adaptation, Physiological↗

Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus.

The role of hybridization in adaptive evolution is contentious. While many cases of adaptive trait introgression have been proposed, the relevant traits have rarely been identified, resulting in a lack of clear examples of this process. Here, we examine a purported case of adaptive introgression in which the annual sunflower Helianthus annuus annuus has captured alleles from a congener (Helianthus debilis) to form a stabilized hybrid, Helianthus annuus texanus. We tested the hypotheses that herbivore resistance traits have introgressed from H. debilis to H. annuus and have increased adaptation in the latter. In two common gardens, fitness (estimated by seed production) was on average 55% higher in H. a. texanus than in H. a. annuus. For H. a. texanus, three damage traits (of seven tested) differed significantly from the H. a. annuus parent in one or both sites and were shifted in the direction of the more resistant H. debilis. Natural selection favored H. a. annuusxH. debilis BC(1) hybrids (synthesized to mimic the ancestors of H. a. texanus) with H. debilis-like resistance to seed midges Neolasioptera helianthis and to receptacle/seed feeding Lepidoptera at one or both sites. Assuming similar herbivore pressures in the past, these results suggest that introgression of biotic resistance traits was important in the adaptation of H. annuus to central and southern Texas.

Adaptation, Biological↗

Rapid adaptation of insect herbivores to an invasive plant.

Introduced plant success often is attributed to release from natural enemies in their new ranges. However, herbivores may accumulate over time and reduce invasiveness but evidence for this process to date is weak. We report here that enemy release is indeed limited to the early stages of introduction of the Chinese tallow tree (Sapium sebiferum). In bioassays and gardens along a geographical gradient of time since tallow tree introduction, herbivory was highest and tree performance was poorest where tallow tree has been present longer (i.e. introduced earlier). Additionally, Asian ecotypes (grown from seeds collected in Asia) had lower survival than North American ecotypes (seeds collected in North America), which is consistent with genetic responses to low herbivory in the introduced range (EICA Hypothesis). Release from insect herbivores appears to contribute to early success of the tallow tree, but accumulation of insect herbivores has apparently reduced this benefit over time.

Adaptation, Physiological↗

How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals?

What digestive adaptations permit herbivorous nonruminant mammals to sustain much higher metabolic rates than herbivorous lizards, despite gross similarity in digestive anatomy and physiology? We approached this question by comparing four herbivorous species eating the same diet of alfalfa pellets: two lizards (chuckwalla and desert iugana) and two mammals (desert woodrat and laboratory mouse). The mammals had longer small and large intestines, greater intestinal surface area, much higher (by an order of magnitude) food intake normalized to metabolic live mass, and much faster food passage times (a few hours instead of a few days). Among both reptiles and mammals, passage times increase with body size and are longer for herbivores than for carnivores. The herbivorous lizards, despite these much slower passage times, had slightly lower apparent digestive efficiencies than the mammals. At least for chuckwallas, this difference from mammals was not due to differences in body temperature regime. Comparisons of chuckwallas and woodrats in their assimilation of various dietary components showed that the woodrat's main advantage lay in greater assimilation of the dietary fiber fraction. Woodrats achieved greater fiber digestion despite shorter residence time, but possibly because of a larger fermentation chamber, coprophagy, and/or different conditions for microbial fermentation. We conclude with a comparative overview of digestive function in herbivorous lizards and mammals, and with a list of four major unsolved questions.

Adaptation, Biological↗

Evolution of specialization and ecological character displacement of herbivores along a gradient of plant quality.

We study the combined evolutionary dynamics of herbivore specialization and ecological character displacement, taking into account foraging behavior of the herbivores, and a quality gradient of plant types. Herbivores can adapt by changing two adaptive traits: their level of specialization in feeding efficiency and their point of maximum feeding efficiency along the plant gradient. The number of herbivore phenotypes, their levels of specialization, and the amount of character displacement among them are the result of the evolutionary dynamics, which is driven by the underlying population dynamics, which in turn is driven by the underlying foraging behavior. Our analysis demonstrates broad conditions for the diversification of a herbivore population into many specialized phenotypes, for basically any foraging behavior focusing use on highest gains while also including errors. Our model predicts two characteristic phases in the adaptation of herbivore phenotypes: a fast character-displacement phase and a slow coevolutionary niche-shift phase. This two-phase pattern is expected to be of wide relevance in various consumer-resource systems. Bringing together ecological character displacement and the evolution of specialization in a single model, our study suggests that the foraging behavior of herbivorous arthropods is a key factor promoting specialist radiation.

Adaptation, Biological↗

Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory.

Literature data were collected on the floristic distribution and toxicity of phytochemicals to herbivores and on herbivore specialization in order to test phytochemical coevolution theory. The theory makes four predictions that can be tested with this information. Herbivores can adapt to novel, more toxic chemicals by becoming specialists, or they can become generalists but at the cost of lower feeding success on any particular host. Thus, the first two predictions are as follows: herbivores should do better on chemicals that are present in their normal host, and this pattern should be stronger for specialists than for generalists. The "escape and radiation" aspect of the theory holds that if a plant taxon with a novel defense chemical diversifies, the chemical will become widespread. Eventually, herbivores will adapt to and disarm it. So the third prediction is that more widespread chemicals are less toxic than more narrowly distributed ones. Because generalists should not do as well as specialists on chemicals disarmed by the latter, the fourth prediction is that the third prediction should be more true for generalists than specialists and should depend on presence/absence of the chemical in the normal host. Multiple regressions of toxicity (herbivore mortality and final weight) on three predictor variables (chemical presence/absence in the normal host, specialism, and chemical floristic distribution) and relevant interactions were used to test these predictions. Chemical presence/absence in the normal host, the interaction between this variable and specialism, and chemical floristic distribution had significant effects on both measures of toxicity, supporting the first three predictions of the model. Support for the fourth prediction (a three-way interaction among all predictor variables) was evident for final weight but not mortality, perhaps because growth is more responsive to toxicity differences than survival. In short, the phytochemistry literature provides broad support for the phytochemical coevolution model.

Adaptation, Physiological↗

Postnatal development of the masseter muscles in the Japanese field vole Microtus montebelli, with special attention to differentiation of the fast-twitch oxidative fiber.

Postnatal development and differentiation of the masseter muscles consisting only of fast-twitch oxidative (FO) fibers in the adult Japanese field vole Microtus montebelli were studied using histochemical and electron microscopic techniques. The masseter muscles were composed of myotubes and muscle fibers at day 0 (birth day). Most muscle cells showed the strong reaction for myosin ATPase after both alkaline and acid preincubations. For NADH-dehydrogenase (NADH-DH), small granular diformazan deposits were recognized in the sarcoplasm. Afterwards, the masseter muscles consisted of myofibers and satellite cells at day 5. For myosin ATPase, weakly-reactive fibers after acid preincubation (fast-twitch fibers) increased in number. For NADH-DH, granular diformazan deposits in all the myofibers increased in size. Since all the myofibers had numerous sarcoplasmic reticula, and they reacted strongly after alkaline preincubation and weakly after acid preincubation for myosin ATPase at day 10 when the young start to take solid food, it seems that the masseter muscles become contractive fast. At day 15 (before weaning), all the myofibers showed the adult-like strong reaction for NADH-DH and had numerous well-developed mitochondria, thus they acquired the ability of the fast and sustained contraction. It is accordingly considered that the masseter muscles of the vole mature in a short time after birth because of adaptation for herbivorous food habit.

Adaptation, Physiological↗

Nutrition of the domestic cat, a mammalian carnivore.

From the foregoing discussion of the nutritional requirements and some of the metabolic anomalies of the cat, it is clear that the cat is adapted to eating a carnivorous diet. It may, however, have less capability than omnivores and herbivores to adapt to wide ranges in dietary composition. For example, the lack of ability to synthesize sufficient vitamin A from carotene, ornithine from glutamic acid, arachidonate from linoleate, and taurine from cysteine results from a complete deletion or severe limitation of the enzyme or pathway that makes each nutrient. Other nutrient requirements, such as the absolute requirement for niacin and the high protein requirement, appear to result from the high activity of one or more enzymes and the fact that these enzymes are not adaptive in the cat. For example, the cat cannot decrease picolinic carboxylase in order to force tryptophan toward the niacin-synthetic pathway (244) nor can it decrease the urea cycle enzymes when dietary protein is decreased in the diet in order to conserve nitrogen (209). Indeed, the cat appears to have less capability to adapt to most changes in dietary composition because it cannot change the quantities of enzymes involved in the metabolic pathways (209). This evolutionary development has resulted in more stringent nutritional requirements for cats than for omnivores such as the rat, dog, and man. What little evidence exists for other carnivore species leads us to suggest that this pattern may well be common among other strict carnivores. The metabolic differences between the cat and omnivores provide the researcher with a useful animal model for studying the biochemical basis of some nutrient requirements. For example, because there is no significant conversion of linoleate to arachidonate in cat liver (101, 150, 231), the physiological functions of linoleate can be determined independent of it having a role as a precursor of arachidonate (150). This has not been possible with other species. It is anticipated that further studies of the nutrition of the cat will increase our understanding of metabolic adaptation and nutrient functions.

Amino Acids↗