How bright and how nasty: explaining diversity in warning signal strength

The conspicuous displays that warn predators of defenses carried by potential prey have been of interest to evolutionary biologists from the time of Wallace and Darwin to the present day. Although most studies implicitly assume that these "aposematic" warning signals simply indicate the presence of some repellent defense such as a toxin, it has been speculated that the intensity of the signal might reliably indicate the strength of defense so that, for example, the nastiest prey might "shout loudest" about their unprofitability. Recent phylogenetic and empirical studies of Dendrobatid frogs provide contradictory views, in one instance showing a positive correlation between toxin levels and conspicuousness, in another showing a breakdown of this relationship. In this paper we present an optimization model, which can potentially account for these divergent results. Our model locates the optimal values of defensive traits that are influenced by a range of costs and benefits. We show that optimal aposematic conspicuousness can be positively correlated with optimal prey toxicity, especially where population sizes and season lengths vary between species. In other cases, optimal aposematic conspicuousness may be negatively correlated with toxicity; this is especially the case when the marginal costs of aposematic displays vary between members of different populations. Finally, when displays incur no allocation costs there may be no single optimum value for aposematic conspicuousness, rather a large array of alternative forms of a display may have equal fitness.     

Warning coloration can be disruptive: aposematic marginal wing patterning in the wood tiger moth

Warning (aposematic) and cryptic colorations appear to be mutually incompatible because the primary function of the former is to increase detectability, whereas the function of the latter is to decrease it. Disruptive coloration is a type of crypsis in which the color pattern breaks up the outline of the prey, thus hindering its detection. This delusion can work even when the prey's pattern elements are highly contrasting; thus, it is possible for an animal's coloration to combine both warning and disruptive functions. The coloration of the wood tiger moth (Parasemia plantaginis) is such that the moth is conspicuous when it rests on vegetation, but when it feigns death and drops to the grass‐ and litter‐covered ground, it is hard to detect. This death‐feigning behavior therefore immediately switches the function of its coloration from signaling to camouflage. We experimentally tested whether the forewing patterning of wood tiger moths could function as disruptive coloration against certain backgrounds. Using actual forewing patterns of wood tiger moths, we crafted artificial paper moths and placed them on a background image resembling a natural litter and grass background. We manipulated the disruptiveness of the wing pattern so that all (marginal pattern) or none (nonmarginal pattern) of the markings extended to the edge of the wing. Paper moths, each with a hidden palatable food item, were offered to great tits (Parus major) in a large aviary where the birds could search for and attack the “moths” according to their detectability. The results showed that prey items with the disruptive marginal pattern were attacked less often than prey without it. However, the disruptive function was apparent only when the prey was brighter than the background. These results suggest that warning coloration and disruptive coloration can work in concert and that the moth, by feigning death, can switch the function of its coloration from warning to disruptive.     

Evidence for aposematism in the plant bug Lopidea nigridea Uhler (Hemiptera: Miridae: Orthotylinae)

The biology of the plant bug Lopidea nigridea is described, with particular focus on whether this red and black species can be considered aposematic. Lopidea individuals were rejected after attack in 92 of 112 feeding trials involving three of their five most common arthropod predator species. Compared to another syntopic plant bug species, L. nigridea is aggregated in distribution, and individuals are sedentary in their basic daily habits. These life-history features, coupled with the ability to survive most attacks by arthropod predators in the feeding trials, suggest that L. nigridea is protected to some degree by an aposematic defence. How L. nigridea may acquire its distastefulness is discussed, with special attention to host plant relations in L. nigridea and in the genus Lopidea as a whole.     

Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

COVARIATION OF DEFENSIVE TRAITS IN TIGER BEETLES (GENUS CICINDELA): A PHYLOGENETIC APPROACH USING mtDNA

Inferences about the evolution of defensive strategies in tiger beetles (genus Cicindela) have been contentious, largely due to the lack of a phylogenetic hypothesis for the group. We used a dataset that includes measures of chemical defense, habitat association, and body coloration for a representative sample of North American Cicindela (Pearson et al. 1988) to reassess, within a phylogenetic context, the problem of covariation in defensive strategies. We reconstructed a phylogenetic hypothesis from mtDNA for a total of 44 Cicindela and seven outgroup taxa using 1896 base pairs from three segments of the mitochondrial genome. Characters involved in predator deterrence and escape were optimized onto this phylogeny. Although most taxa producing large amounts of benzaldehyde fall into two monophyletic clades, numerous changes in the level of benzaldehyde secretion across the genus suggest that this parameter is poorly conserved phylogenetically. In contrast to previous studies, we also found little support for correlated character changes in benzaldehyde secretion and habitat type, a presumed indicator of the selective regime. Aposematic coloration of the abdomen was restricted to a single monophyletic group of taxa producing large amounts of benzaldehyde. Bright iridescent coloration, implicated in predator evasion during flight, was only loosely correlated with the phylogenetic affinities of taxa and appears to be part of a defensive strategy not usually acting in combination with chemical defenses. Our study of character covariation clarifies earlier analyses of the adaptive significance of benzaldehyde defense, which were inconclusive without a phylogenetic hypothesis.     

PHYLOGENETIC TRENDS IN PHENOLIC METABOLISM OF MILKWEEDS (ASCLEPIAS): EVIDENCE FOR ESCALATION

Although plant-defense theory has long predicted patterns of chemical defense across taxa, we know remarkably little about the evolution of defense, especially in the context of directional phylogenetic trends. Here we contrast the production of phenolics and cardenolides in 35 species of milkweeds ( Asclepias and Gomphocarpus ). Maximum-likelihood analyses of character evolution revealed three major patterns. First, consistent with the defense-escalation hypothesis, the diversification of the milkweeds was associated with a trend for increasing phenolic production; this pattern was reversed (a declining evolutionary trend) for cardenolides, toxins sequestered by specialist herbivores. Second, phylogenetically independent correlations existed among phenolic classes across species. For example, coumaric acid derivatives showed negatively correlated evolution with caffeic acid derivatives, and this was likely driven by the fact that the former are used as precursors for the latter. In contrast, coumaric acid derivatives were positively correlated with flavonoids, consistent with competition for the precursor p- coumaric acid. Finally, of the phenolic classes, only flavonoids showed correlated evolution (positive) with cardenolides, consistent with a physiological and evolutionary link between the two via malonate. Thus, this study presents a rigorous test of the defense-escalation hypothesis and a novel phylogenetic approach to understanding the long-term persistence of physiological constraints on secondary metabolism.     

Toward a more trait-centered approach to diffuse (co)evolution

How species evolve depends on the communities in which they are embedded. Here, we briefly review the ideas underlying concepts of diffuse coevolution, evolution, and selection. We discuss criteria to identify when evolution will be diffuse. We advocate a more explicitly trait-oriented approach to diffuse (co)evolution, and discuss how considering effects of interacting species on fitness alone tells us little about evolution. We endorse the view that diffuse evolution occurs whenever the response to selection by one interacting species on a given trait is altered by the presence of a second interacting species. Building on the work of others, we clarify and expand the criteria for diffuse evolution and present a simple experimental design that will allow the detection of diffuse selection. We argue that a greater focus on selection on specific traits and the evolutionary response to that selection will improve our conceptual understanding of how communities affect the evolution of species embedded within them.     

Reactions of green lizards (Lacerta viridis) to major repellent compounds secreted by Graphosoma lineatum (Heteroptera: Pentatomidae)

The chemical defence of Heteroptera is primarily based on repellent secretions which signal the potential toxicity of the bug to its predators. We tested the aversive reactions of green lizards (Lacerta viridis) towards the major compounds of the defensive secretion of Graphosoma lineatum, specifically: (i) a mixture of three aldehydes: (E)-hex-2-enal, (E)-oct-2-enal, (E)-dec-2-enal; (ii) a mixture of these three aldehydes and tridecane; (iii) oxoaldehyde: (E)-4-oxohex-2-enal; (iv) secretion extracted from metathoracic scent glands of G. lineatum adults and (v) hexane as a non-polar solvent. All chemicals were presented on a palatable food (Tenebrio molitor larvae). The aversive reactions of the green lizards towards the mealworms were evaluated by observing the approach latencies, attack latencies and approach–attack intervals. The green lizards exhibited a strong aversive reaction to the mixture of three aldehydes. Tridecane reduced the aversive reaction to the aldehyde mixture. Oxoaldehyde caused the weakest, but still significant, aversive reaction. The secretion from whole metathoracic scent glands also clearly had an aversive effect on the green lizards. Moreover, when a living specimen of G. lineatum or Pyrrhocoris apterus (another aposematic red-and-black prey) was presented to the green lizards before the trials with the aldehyde mixture, the aversive effect of the mixture was enhanced. In conclusion, the mixture of three aldehydes had the strong aversive effect and could signal the potential toxicity of G. lineatum to the green lizards.     

Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae)

Zhang, G. and Weirauch, C. 2011. Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). —Acta Zoologica (Stockholm) 00 : 1–10. For more than 50 years, specialized dermal glands that secrete sticky substances and specialized setae have been known from the legs of New World assassin bugs in the genus Zelus Fabricius (Reduviidae: Harpactorinae). The gland secretions and specialized ‘sundew setae’ are involved in enhancing predation success. We here refer to this predation strategy as ‘sticky trap predation’ and the specialized dermal glands as ‘sticky glands’. To determine how widespread sticky trap predation is among Reduviidae, we investigated taxonomic distribution of sticky glands and sundew setae using compound light microscopical and scanning electron microscopical techniques and sampling 67 species of Reduviidae that represent 50 genera of Harpactorini. We found sticky glands in 12 genera of Harpactorini and thus show that sticky trap predation is much more widespread than previously suspected. The sticky glands vary in shape, size and density, but are always located in a dorsolateral position on the fore tibia. Sundew setae are present in all taxa with sticky glands with the exception of Heza that instead possesses unique lamellate setae. The sticky trap predation taxa are restricted to the New World, suggesting a New World origin of this unique predation strategy.     

Docking proteins and peptides under evolutionary constraints in Critical Assessment of PRediction of Interactions rounds 38 to 45

Computational structural prediction of macromolecular interactions is a fundamental tool toward the global understanding of cellular processes. The Critical Assessment of PRediction of Interactions (CAPRI) community-wide experiment provides excellent opportunities for blind testing computational docking methods and includes original targets, thus widening the range of docking applications. Our participation in CAPRI rounds 38 to 45 enabled us to expand the way we include evolutionary information in structural predictions beyond our standard free docking InterEvDock pipeline. InterEvDock integrates a coarse-grained potential that accounts for interface coevolution based on joint multiple sequence alignments of two protein partners (co-alignments). However, even though such co-alignments could be built for none of the CAPRI targets in rounds 38 to 45, including host-pathogen and protein-oligosaccharide complexes and a redesigned interface, we identified multiple strategies that can be used to incorporate evolutionary constraints, which helped us to identify the most likely macromolecular binding modes. These strategies include template-based modeling where only local adjustments should be applied when query-template sequence identity is above 30% and larger perturbations are needed below this threshold; covariation-based structure prediction for individual protein partners; and the identification of evolutionarily conserved and structurally recurrent anchoring interface motifs. Overall, we submitted correct predictions among the top 5 models for 12 out of 19 interface challenges, including four High- and five Medium-quality predictions. Our top 20 models included correct predictions for three out of the five targets we missed in the top 5, including two targets for which misleading biological data led us to downgrade correct free docking models.     

The Labeninae (Hymenoptera: Ichneumonidae): a study in phylogenetic reconstruction and evolutionary biology

The internal phylogenetic relationships of the ichneumonid subfamily Labeninae (Hymenoptera) are re‐assessed using 136 characters for 54 species representing all currently known species‐groups. New character sets are used. These include a new form of seta (named the grossulariform setae) which are present on the inner surface of the hind coxa of some females, and the extensive structural modifications of the terminal segments of the female metasoma, which are described and structural homologies established. The monophyly of the Labeninae and of the four component tribes, Groteini, Poecilocryptini, Xenothyrini and Labenini, is demonstrated. The Groteini is shown to be the sister‐group to the Poecilocryptini + (Xenothyrini + Labenini). Monophyletic genera are established, including three new genera: Ozlabium gen. nov. Gauld & Wahl (type‐species 0. arcadium sp. nov.) in the Groteini from Australia; Torquinsha gen. nov. Gauld & Wahl (type‐species Certonotus invictus Porter) in the Labenini from Chile, and Gauldianus gen. nov. Lanfranco (type‐species Gauldianus chilensis sp. nov. Lanfranco) in the Labenini from Chile. Apechoneura is removed from synonymy and re‐instated as a valid genus for a complex of tropical American species. The biogeographic patterns shown by the Labeninae are discussed. Evidence suggests that the group radiated on Gondwanaland after the separation of Africa/India/Madagascar, but prior to the separation of Australia. Species occurring off the southern continental fragments, in North America, are shown to be members of highly derived lineages, a result consistent with the hypothesis that labenines colonized North America recently through Mesoamerica. Patterns of host utilization and mating behaviour are examined for the group. Members of the more derived lineages show progressively more female specializations for attacking hosts deeply concealed in woody substrates. Males in the more specialized lineages are shown to have a wider array of secondary sexual characteristics and genitalic ornamentations than more plesiomorphic taxa.     

The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae)

A review of data on the background of wing dimorphism in carabid beetles (Coleoptera: Carabidae) and especially of the closely relatedCalathus cinctus andC. melanocephalus is given. In bothCalathus species wing dimorphism is inherited in a simple Mendelian fashion with the brachypterous condition dominant, but inC. melanocephalus the expression of the long winged genotype is under environmental control as well. The development of long winged phenotypes in the latter species is favoured by relatively favourable environmental conditions, such as high temperatures and a high food-supply. The higher fecundity of the larger and heavier long winged females of both species may compensate for losses of long winged phenotypes by flight activities. The evolutionary significance of both types of inheritance is discussed in relation to dispersal. The ‘fixed type’ as found inC. cinctus is considered an opportunistic short term ‘between sites strategy’, whereas the ‘dynamic type’ ofC. melanocephalus represents a flexible long term ‘within sites strategy’.     

Selection of sleeping trees in pileated gibbons (Hylobates pileatus)

Selection and use patterns of sleeping sites in nonhuman primates are suggested to have multiple functions, such as predation avoidance, but they might be further affected by range defense as well as foraging constraints or other factors. Here, we investigate sleeping tree selection by the male and female members of one group of pileated gibbons (Hylobates pileatus) at Khao Ang Rue Nai Wildlife Sanctuary, Thailand. Data were collected on 113 nights, between September 2006 and January 2009, yielding data on 201 sleeping tree choices (107 by the female and 94 by the male) and on the characteristics of 71 individual sleeping trees. Each sleeping tree and all trees ≥40 cm diameter at breast height (DBH) in the home range were assessed (height, DBH, canopy structure, liana load) and mapped using a GPS. The gibbons preferentially selected tall (mean=38.5 m), emergent trees without lianas. The majority of the sleeping trees (53.5%) were used only once and consecutive reuse was rare (9.5%). Sleeping trees were closer to the last feeding tree of the evening than to the first feeding tree in the morning, and sleeping trees were located in the overlap areas with neighbors less often than expected based on time spent in these areas. These results suggest avoidance of predators as the main factor influencing sleeping tree selection in pileated gibbons. However, other non‐mutually exclusive factors may be involved as well. Am. J. Primatol. 72:617–625, 2010. © 2010 Wiley‐Liss, Inc.     

Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies

Conclusions Contrasting effects of generalist and specialist herbivores can explain why all plants have not evolved high levels of defence. Maintenance of variation in concentration of defence substances can be explained by a shifting balance between natural selection for defence against herbivory by specialists and generalists. Generalist natural enemies will shift the optimal defence curve to lower concentrations of defences. Physiological costs of production of defence substances and selection by specialist herbivores of plant phenotypes with higher levels of defence compounds for sequestration are no essential elements of this model. They may, however, adjust the predicted optimum defence function and contribute to maintenance of variation of concentrations of defence substances.     

小黑瓢虫对高氏瘤粉虱捕食作用的研究

在高氏瘤粉虱不同虫态共存的条件下,小黑标虫对高氏瘤粉虱各虫态的选择次序为卵＞1龄若虫＞2龄若虫＞3龄若虫＞4龄若虫和拟蛹,对卵的捕食率均最高,有明显的嗜好选择;小黑瓢虫幼虫捕食粉虱卵的数量,随着龄期的增长而递增,其中4龄幼虫的捕食量最大,4龄期捕食量平均为1565．42粒,占全幼虫期总食卵量的45．42％,整个幼虫期可捕食高氏瘤粉虱的卵数平均为3446．5粒。小黑瓢虫3龄幼虫对粉虱卵的捕食作用率在所给的猎物密度（1500粒／皿）条件下,随着自身密度的增加而降低。     

Aggression and fitness differences between plumage morphs in the common buzzard (Buteo buteo)

Genetic plumage polymorphism in birds is increasingly recognizedas a potentially important trait influencing birds’ lifehistories. In the common buzzard Buteo buteo, the 3 color morphsvary in lifetime reproductive success (LRS), but the proximatemechanisms leading to these differences are unknown. We firstconfirmed the stability of the fitness differences found previously,using a greatly extended LRS data set. To find potential causesfor these differences, we experimentally studied variation inaggressive behavior of the morphs, both against an interspecificpredator and intraspecific competitors. The morphs showed substantialvariation in aggressive behavior. Light-colored males were mostaggressive toward an interspecific predator, followed by intermediateand dark males. In females, this pattern was reversed, resultingin sex-related differences of aggression in 2 morphs. When defendingtheir territory against intraspecific competitors, no absolutedifference in aggression was found, but the morphs reacted strongesttoward intruders of a morph similar to their own. This suggeststhat aggression differs both between and within morphs, leadingto a complex pattern on the population level. Coupled with thestrong fitness differences, our results suggest that the geneticbasis of the polymorphism has far-reaching behavioral consequences.     

Island evolutionary biogeography: analysis of the weevils (Coleoptera: Curculionidae) of the Falkland Islands (Islas Malvinas)

Aim I analysed distributional and phylogenetic information on weevils (Coleoptera: Curculionidae) from the Falklands, and integrated it with molecular, palaeontological and geological information to infer a geobiotic scenario. Location Falkland Islands (Islas Malvinas). Methods The panbiogeographical analysis was based on data on 23 Falkland species and their related taxa from southern South America. For the cladistic biogeographical analysis I analysed six weevil taxa for which phylogenetic hypotheses are available (the generic groups Cylydrorhinus, Strangaliodes and Falklandius, and the genera Antarctobius, Germainiellus and Puranius). Results from this analysis were compared with previous regionalizations. Cenocrons (sets of taxa that share the same biogeographical history) were identified by considering temporal information provided by fossils and molecular clocks. Finally, a geobiotic scenario was proposed by integrating the available information. Results Six generalized tracks were detected: Maule–Valdivian forests, Magellanic forest, Magellanic moorland, Falkland Islands, Magellanic forest–Magellanic moorland, and Magellanic forest–Falkland Islands. A node was identified in the Magellanic forest, based on the overlap of two generalized tracks. A single general area cladogram was obtained, implying the following sequence: (Magellanic moorland (Maule–Valdivian forests (Magellanic forest, Falkland Islands))). The Falklands are classified here as a biogeographical province in the Austral realm, Andean region and Subantarctic subregion. Falkland weevils seem to belong to a single Subantarctic cenocron. The sequence of events deduced implies the following steps: development of the Subantarctic biota in southern South America, arrival of the Falkland crustal block from South Africa in the Early Cretaceous, geodispersal of the Subantarctic cenocron from southern South America to the Falklands during the Early Oligocene, vicariance of the Magellanic moorland, vicariance of the Maule–Valdivian forests, and final vicariance between the Magellanic forest and the Falkland Islands. Main conclusions The biotic components identified support the connection of the Falkland weevils with the Magellanic forest. Falkland weevils belong to a single cenocron, dated to at least the Early Oligocene, when geodispersal from southern South America may have occurred. An older African cenocron may have been replaced completely by the Subantarctic one when the proto‐Falklands made contact with the Patagonian continental shelf. A geobiotic scenario implying vicariance events related to sea‐level variations could explain the distributional patterns analysed herein.