Selection Mosaic Exerted by Specialist and Generalist Herbivores on Chemical and Physical Defense of Datura stramonium

Selection exerted by herbivores is a major force driving the evolution of plant defensive characters such as leaf trichomes or secondary metabolites. However, plant defense expression is highly variable among populations and identifying the sources of this variation remains a major challenge. Plant populations are often distributed across broad geographic ranges and are exposed to different herbivore communities, ranging from generalists (that feed on diverse plant species) to specialists (that feed on a restricted group of plants). We studied eight populations of the plant Datura stramonium usually eaten by specialist or generalist herbivores, in order to examine whether the pattern of phenotypic selection on secondary compounds (atropine and scopolamine) and a physical defense (trichome density) can explain geographic variation in these traits. Following co-evolutionary theory, we evaluated whether a more derived alkaloid (scopolamine) confers higher fitness benefits than its precursor (atropine), and whether this effect differs between specialist and generalist herbivores. Our results showed consistent directional selection in almost all populations and herbivores to reduce the concentration of atropine. The most derived alkaloid (scopolamine) was favored in only one of the populations, which is dominated by a generalist herbivore. In general, the patterns of selection support the existence of a selection mosaic and accounts for the positive correlation observed between atropine concentration and plant damage by herbivores recorded in previous studies.     

Reliance on pollinators predicts defensive chemistry across tobacco species

Defensive traits are typically studied in the context of avoiding antagonists, but may also mediate key interactions with mutualists. Plant chemical defences occur in flowers, suggesting pollinators may be agents of selection on defence. We hypothesised that floral defences would deter pollinators, and therefore, pollinators would select for lower defences in outcrossing than self-pollinating species. We measured pollinator reliance and alkaloid levels in 32 greenhouse-grown Nicotiana species. Using a comparative phylogenetic approach, we found significantly lower nectar, floral and leaf nicotine concentrations in outcrossing than selfing species, with a 15-fold decrease in leaf nicotine levels. Nicotine concentrations were positively correlated across tissues, suggesting that selection against floral defences could constrain the evolution of leaf defences. Thus, pollinators could shape the evolution not only of floral defences but also of defences in other tissues where herbivores have traditionally been considered the dominant agent of selection.     

Evolution of extrafloral nectaries: adaptive process and selective regime changes from forest to savanna

Much effort has been devoted to understanding the function of extrafloral nectaries (EFNs) for ant–plant–herbivore interactions. However, the pattern of evolution of such structures throughout the history of plant lineages remains unexplored. In this study, we used empirical knowledge on plant defences mediated by ants as a theoretical framework to test specific hypotheses about the adaptive role of EFNs during plant evolution. Emphasis was given to different processes (neutral or adaptive) and factors (habitat change and trade‐offs with new trichomes) that may have affected the evolution of ant–plant associations. We measured seven EFN quantitative traits in all 105 species included in a well‐supported phylogeny of the tribe Bignonieae (Bignoniaceae) and collected field data on ant–EFN interactions in 32 species. We identified a positive association between ant visitation (a surrogate of ant guarding) and the abundance of EFNs in vegetative plant parts and rejected the hypothesis of phylogenetic conservatism of EFNs, with most traits presenting K‐values < 1. Modelling the evolution of EFN traits using maximum likelihood approaches further suggested adaptive evolution, with static‐optimum models showing a better fit than purely drift models. In addition, the abundance of EFNs was associated with habitat shifts (with a decrease in the abundance of EFNs from forest to savannas), and a potential trade‐off was detected between the abundance of EFNs and estipitate glandular trichomes (i.e. trichomes with sticky secretion). These evolutionary associations suggest divergent selection between species as well as explains K‐values < 1. Experimental studies with multiple lineages of forest and savanna taxa may improve our understanding of the role of nectaries in plants. Overall, our results suggest that the evolution of EFNs was likely associated with the adaptive process which probably played an important role in the diversification of this plant group.     

IS SPECIALIZATION A DEAD END? THE PHYLOGENY OF HOST USE IN DENDROCTONUS BARK BEETLES (SCOLYTIDAE)

Ecological explanations for the prevalence of resource specialists are abundant, whereas phylogenetic evidence on their origins is scarce. In this paper, we provide a molecular phylogenetic study of the 19 specialist or generalist species in the bark beetle genus Dendroctonus, which collectively attack species in four different genera in the conifer family Pinaceae. Given substantial variation in diet breadth, we asked two general questions concerning the evolution of resource use in this group. How conservative is the evolution of host use in these insects? Does specialization tend to be derived (i.e., a “dead end”)? To answer these questions, we estimated the phylogeny of Dendroctonus using mitochondrial DNA sequences and mapped transitions in resource use on the resulting phylogeny estimate. The evolution of affiliations with Pinus and Picea hosts in Dendroctonus was conservative among beetle species (PTP test; P < 0.012), but there was no significant correspondence between the phylogeny of these beetles and the phylogeny among their Pinaceae hosts (among genera, P = 0.28; among Pinus species, P = 0.82). Degree of specialization, as measured in the proportion of hosts used, was bimodally distributed with “generalist” species utilizing < 60% of the congeneric hosts within their range and six specialist species utilizing < 40% of the available hosts. Among the generalists, we found a strong correlation between the number of hosts encountered and the number of hosts utilized (R = 0.97, P < 0.0001), whereas there was no significant correlation among the specialists (R = 0.27, P = 0.59). The evolution of specialization in Dendroctonus proved highly labile—specialists arose from generalists at least six separate times (without reversal) all in derived positions, and closer examination of some specialists revealed instances where they appear to have lost particular host species from their diet. However, evidence from the ecological literature also suggests that several Dendroctonus generalists may have increased their range of host genera within the Pinaceae.     

Movement ecology of Afrotropical birds: Functional traits provide complementary insights to species identity

Effects of anthropogenic activities on habitats and species communities and populations are complex and vary across species depending on their ecological traits. Movement ecology may provide important insights into species’ responses to habitat structures and quality. We investigated how movement behavior across a human‐modified landscape depends on species identity and species traits, with particular focus on habitat specialization, feeding guilds, and dispersal behavior. We tracked 34 individuals of nine Afrotropical bird species during three years in an anthropogenic riparian landscape of East Africa. We investigated whether species’ functional traits predicted their habitat use and movement behavior better than species’ identities. Our results indicate that habitat specialists mainly occur in dense riparian thickets, while habitat generalists do occur in agricultural land. Home‐ranges of omnivorous habitat generalists are larger than of frugivorous and insectivorous generalists and omnivorous and insectivorous specialists. Movement speed was highest in settlement areas for all species, with activity peaks during morning and afternoon for habitat specialists. Our results reveal that functional traits and species identity provide complementary insights into responses of organisms to habitat structures and habitat quality.     

Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist–specialist trade‐offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade‐offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31 °C) or a cold (15 °C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life‐history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature‐mediated trade‐off between juvenile survival and size at maturity, suggesting that trade‐offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist–specialist dimension.     

Elevational gradients in constitutive and induced oak defences based on individual traits and their correlated expression patterns

Elevational gradients are useful ecological settings for revealing the biotic and abiotic drivers of plant trait variation and plant–insect interactions. However, most work focusing on plant defences has looked at individual traits and few studies have assessed multiple traits simultaneously, their correlated expression patterns, and abiotic factors associated with such patterns across elevations. To address this knowledge gap, we studied elevational variation in direct (phenolic compounds) and indirect (volatile organic compounds) constitutive defences and their inducibility after feeding by a specialist beetle Altica quercetorum in saplings of 18 wild populations of Quercus pyrenaica. We tested for: 1) clines in each defensive trait individually, 2) their patterns of correlated expression and 3) associations between any such clines and climatic factors. We found that constitutive direct defences (lignins and hydrolysable tannins) decreased with increasing elevation. We observed no elevational gradient for constitutive indirect defences (volatile organic compounds) or the inducibility of direct or indirect defensive traits when looking at groups of compounds. However, at individual tree-level, increased induction of two monoterpenes (α-fenchene and camphene) at higher elevation was shown. Furthermore, we show a significant pattern of co-expression of constitutive and induced phenolics across populations, which weakened with increasing elevation. Finally, we found no evidence that climatic factors were associated with either individual or correlated trait expression patterns across elevations. Overall, these findings call for moving beyond elevational clines in individual plant defences, and argue that assessing elevational shifts in trait correlated expression patterns and their underlying mechanisms can increase our understanding of plant defence evolution and plant–herbivore interactions along environmental gradients.     

How insects overcome two‐component plant chemical defence: plant β‐glucosidases as the main target for herbivore adaptation

Insect herbivory is often restricted by glucosylated plant chemical defence compounds that are activated by plant β‐glucosidases to release toxic aglucones upon plant tissue damage. Such two‐component plant defences are widespread in the plant kingdom and examples of these classes of compounds are alkaloid, benzoxazinoid, cyanogenic and iridoid glucosides as well as glucosinolates and salicinoids. Conversely, many insects have evolved a diversity of counter‐adaptations to overcome this type of constitutive chemical defence. Here we discuss that such counter‐adaptations occur at different time points, before and during feeding as well as during digestion, and at several levels such as the insects' feeding behaviour, physiology and metabolism. Insect adaptations frequently circumvent or counteract the activity of the plant β‐glucosidases, bioactivating enzymes that are a key element in the plant's two‐component chemical defence. These adaptations include host plant choice, non‐disruptive feeding guilds and various physiological adaptations as well as metabolic enzymatic strategies of the insect's digestive system. Furthermore, insect adaptations often act in combination, may exist in both generalists and specialists, and can act on different classes of defence compounds. We discuss how generalist and specialist insects appear to differ in their ability to use these different types of adaptations: in generalists, adaptations are often inducible, whereas in specialists they are often constitutive. Future studies are suggested to investigate in detail how insect adaptations act in combination to overcome plant chemical defences and to allow ecologically relevant conclusions.     

Tibor Jermy (1917–2014)

Throughout the course of their evolution, plants have acquired a wide range of chemical and mechanical defenses to protect against herbivores. Ehrlich & Raven's coevolutionary theory suggests that this diversification of defensive traits is driven by the strong impact of novel traits on insect herbivores. However, the impact of plant defenses on insects is difficult to compare between related plant species due to variation in environmental and biotic conditions. We standardized these factors as far as possible by analyzing the effects of chemical and mechanical defensive traits on insects in a local community of 11 Salicaceae species growing in sympatry, and their leaf‐chewing herbivores. Defensive traits (salicylates, flavonoids, tannins, trichomes, and leaf toughness) were generally not inter‐correlated, with the exception of a negative correlation between salicylates and trichomes. The content of salicylates, a novel group of defensive metabolites in the Salicaceae, was correlated with low herbivore diversity and high host specificity. Despite these effects, the phylogeny of the studied species shows loss of salicylates in some Salix species instead of their further diversification. This could be due to salicylates not decreasing the overall abundance of herbivores, despite accounting for up to 22% of the dry leaf mass and therefore being costly. The defense of low‐salicylate willow species is thus probably maintained by other defensive traits, such as trichomes. Our study shows that the balance between costs and benefits of defensive traits is not necessarily in favor of novel compounds and illustrates a process, which may lead to the reduction in a defensive trait.     

Is there rapid evolutionary response in introduced populations of tansy ragwort, <Emphasis Type="Italic">Jacobaea vulgaris</Emphasis>, when exposed to biological control?

Differences in the herbivore community between a plant’s native (specialists and generalists) and introduced range (almost exclusively generalists) may lead to the evolution of reduced allocation to defences against specialist herbivores in the introduced range, allowing for increased allocation to competitive ability and to defences against generalist herbivores. Following this logic, the introduction of biological control agents should reverse this evolutionary shift and select for plants with life-history traits that are more similar to those of plants in the native range than those of plants in the introduced range that have not been exposed to biological control. In a common garden experiment, we compared performance and resistance traits of tansy ragwort, Jacobaea vulgaris, among populations from the introduced range (New Zealand and North America) that have either been exposed to or grown free from the biological control agent Longitarsus jacobaeae. For comparison, we included populations from the native European range. We found lower levels of generalist-deterrent pyrrolizidine alkaloids (PAs) and of soluble phenolics in New Zealand populations with than in populations without exposure to L. jacobaeae, while the opposite pattern was detected among North American populations. Contrary to expectation, populations with exposure to L. jacobaeae revealed more feeding damage by L. jacobaeae than populations without exposure. Introduced populations had higher levels of PAs and reproductive output than native J. vulgaris populations. Jacobaea vulgaris was introduced in different parts of the world some 100–130 years ago, while L. jacobaeae was introduced only some 20–40 years ago. Hence, the larger differences observed between native and introduced populations, as compared to introduced populations with and without biological control history, may result from different time scales available for selection to act.     

Dynamic trait-niche relationships shape niche partitioning across habitat transformation gradients

Multidimensional approaches examining complex trait-niche relationships are crucial to understand community assembly. This is particularly important across habitat transformation gradients because specialists are progressively substituted by generalists and, despite increasing functional homogenization, in both specialist and generalist communities niche partitioning is apparent. Here, in line with the continuum hypothesis, we expected that divergent trait-niche relationships would arise in passerine assemblages across the natural-to-urban transformation gradient. More specifically, we expected that traits linking form to function would be more important in less transformed habitats, while population density and traits linked to dispersal and dominance would predominate in more transformed habitats. Accordingly, we found that beak length and its interaction with tarsus length correlated significantly with isotopic niches in natural and rural habitats, where specialists predominate. Conversely, body size and aggressiveness only showed significant relationships with isotopic niches with increasing habitat transformation, where generalists prevail. Interestingly, we recorded a mix of these processes in rural habitats, which acted as a frontier between these two domains. Our study is thus important in showing that a complex combination of morphological and behavioral traits determine niche characteristics, and that these relationships are dynamic across habitat transformation gradients.     

Ecology has contrasting effects on genetic variation within species versus rates of molecular evolution across species in water beetles

Comparative analysis is a potentially powerful approach to study the effects of ecological traits on genetic variation and rate of evolution across species. However, the lack of suitable datasets means that comparative studies of correlates of genetic traits across an entire clade have been rare. Here, we use a large DNA-barcode dataset (5062 sequences) of water beetles to test the effects of species ecology and geographical distribution on genetic variation within species and rates of molecular evolution across species. We investigated species traits predicted to influence their genetic characteristics, such as surrogate measures of species population size, latitudinal distribution and habitat types, taking phylogeny into account. Genetic variation of cytochrome oxidase I in water beetles was positively correlated with occupancy (numbers of sites of species presence) and negatively with latitude, whereas substitution rates across species depended mainly on habitat types, and running water specialists had the highest rate. These results are consistent with theoretical predictions from nearly-neutral theories of evolution, and suggest that the comparative analysis using large databases can give insights into correlates of genetic variation and molecular evolution.     

Specialist and generalist herbivores exert opposing selection on a chemical defense

* Plant defense traits often show high levels of genetic variation, despite clear impacts on plant fitness. This variation may be partly maintained by trade-offs in the defense against multiple herbivore species, for example between generalists and coevolved specialists. Despite a long-standing discussion in the literature on the subject, no study to date has specifically manipulated specialist and generalist herbivores independently of one another to determine whether the two guilds exert opposing selection pressures on specific defensive traits. * In two separate experiments, the dominant specialist and generalist herbivores of Brassica nigra were independently manipulated to test whether the composition of the herbivore community altered the direction of selection on a major defensive trait of the plant, sinigrin concentration. * It was found that generalist damage was negatively correlated but specialist loads were positively correlated with increasing sinigrin concentrations; and sinigrin concentration was favored when specialists were removed, disfavored (past an intermediate point) when generalists were removed and selectively neutral when plants faced both generalists and specialists.     

TEMPORAL VARIATION FAVORS THE EVOLUTION OF GENERALISTS IN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade‐offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments.     

Genetic and phenotypic influences on clone-level success and host specialization in a generalist parasite

Studying resource specialization at the individual level can identify factors constraining the evolution of generalism. We quantified genotypic and phenotypic variability among infective stages of 20 clones of the parasitic trematode Maritrema novaezealandensis and measured their infection success and post-infection fitness (growth, egg output) in several crabs and amphipods. First, different clones varied in their infection success of different crustaceans. Second, neither genetic nor phenotypic traits had consistent effects on infection success across all host species. Although the results suggest a relationship between infection success and phenotypic variability, phenotypically variable clones were not better at infecting more host species than less variable ones. Third, genetic and phenotypic traits also showed no consistent correlations with post-infection fitness measures. Overall, we found no consistent clone-level specialization, with some clones acting as specialists and others, generalists. The trematode population therefore maintains an overall generalist strategy by comprising a mixture of clone-level specialists and generalists.     

Plasticity in the expression of direct and indirect defence traits of young plants of <Emphasis Type="Italic">Mallotus japonicus</Emphasis> in relation to soil nutritional conditions

Although soil nutrients can influence the defence strategy of plants that have multiple defence traits, to date, there have been few studies to examine this. To evaluate the effect of soil nutrients on multiple plant defences, we cultivated Mallotus japonicus under three soil nutritional conditions in the field, and experimentally examined the expression of a physical defence trait (trichomes), chemical traits (pellucid dots), and biotic traits (extrafloral nectaries (EFNs) and pearl bodies) of the plants, and the number of ants visiting them. Under the low soil nutritional condition, plants strongly expressed the physical defence by trichomes and chemical defence by pellucid dots, meaning that the young plants adopted direct defences under the poor soil nutritional condition. Under the high soil nutritional condition, in contrast, the plants strongly expressed the indirect defence traits. They produced abundant EFNs and pearl bodies, and attracted many ants. These results suggest that young plants of M. japonicus use different defence modes in response to different soil nutritional conditions.     

No ecological opportunity signal on a continental scale? Diversification and life‐history evolution of African true toads (Anura: Bufonidae)

The niche‐filling process predicted by the “ecological opportunity” (EO) model is an often‐invoked mechanism for generating exceptional diversity in island colonizers. Whether the same process governs lineage accumulation and trait disparity during continental colonization events is less clear. Here, we test this prediction by investigating the rate dynamics and trait evolution of one of Africa's most widespread amphibian colonizers, the true toads (Bufonidae). By reconstructing the most complete molecular phylogeny of African Bufonidae to date, we find that the diversification of lineages in Africa best conforms to a constant rate model throughout time and across subclades, with little support for EO. Evolutionary rates of life‐history traits have similarly been constant over time. However, an analysis of generalists and specialists showed a shift toward higher speciation rates associated with habitat specialization. The overall lack of EO signal can be interpreted in a number of ways and we propose several explanations. Firstly, methodological issues might preclude the detection of EO. Secondly, colonizers might not experience true EO conditions and due to the size, ecological heterogeneity and age of landmasses, the diversification processes might be more complex. Thirdly, lower speciation rates of habitat generalists may have affected overall proliferation of lineages.     

Pollen specialisation is associated with later phenology in Osmia bees (Hymenoptera: Megachilidae)

1. Species exhibit a range of specialisation in diet and other niche axes, with specialists typically thought to be more efficient in resource use but more vulnerable to extinction than generalists. Among herbivorous insects, dietary specialists seem more likely to lack acceptable host plants during the insect's feeding stage, owing to fluctuations in host-plant abundance or phenology. Like other herbivores, bee species vary in host breadth from pollen specialisation (oligolecty) to generalisation (polylecty).
2. Several studies have shown greater interannual variation in flowering phenology for earlier-flowering plants than later-flowering plants, suggesting that early-season bees may experience substantial year-to-year variation in the floral taxa available to them.
3. It was therefore reasoned that, among bees, early phenology could be a more viable strategy for generalists, which can use resources from multiple floral taxa, than for specialists. Consequently, it was expected that the median dates of collection of adult specimens to be earlier for generalist species than for specialists. To test this, phenology data and pollen diet information on 67 North American species of the bee genus Osmia was obtained.
4. Controlling for latitude and phylogeny, it was found that dietary generalisation is associated with significantly earlier phenology, with generalists active, on average, 11–14 days earlier than specialists.
5. This result is consistent with the generalist strategy being more viable than the specialist strategy for species active in early spring, suggesting that dietary specialisation may constrain the evolution of bee phenology—or vice versa.

     

Parallel and non‐parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus)

Parallel phenotypic evolution occurs when independent populations evolve similar traits in response to similar selective regimes. However, populations inhabiting similar environments also frequently show some phenotypic differences that result from non‐parallel evolution. In this study, we quantified the relative importance of parallel evolution to similar foraging regimes and non‐parallel lake‐specific effects on morphological variation in European whitefish (Coregonus lavaretus). We found evidence for both lake‐specific morphological characteristics and parallel morphological divergence between whitefish specializing in feeding on profundal and littoral resources in three separate lakes. Foraging specialists expressed similar phenotypes in different lakes in both overall body shape and selected measured morphological traits. The morphology of the two whitefish specialists resembled that predicted from other fish species, supporting the conclusion of an adaptive significance of the observed morphological characteristics. Our results indicate that divergent natural selection resulting from foraging specialization is driving and/or maintaining the observed parallel morphological divergence. Whitefish in this study may represent an early stage of divergence towards the evolution of specialized morphs.     

Contrasting leaf age preferences of specialist and generalist stick insects (Phasmida)

Specialist and generalist herbivores may select for different types of plant defences or for different distribution of defences within a plant: e.g. between early and late stages of leaf maturation. The differentiation of age-specific defences is particularly pronounced in tropical rain forests where young leaves are often produced year-round, but effects on feeding choices of tropical herbivores are largely unknown. We compared feeding preferences of four species of tropical stick insects (Phasmida) between young or old leaves in dual choice experiments. Two phasmid species ( Haaniella echinata , Lonchodes cultratolobatus ) were highly polyphagous generalists. The other two species were classified as specialists, with Asceles margaritatus feeding mainly on Mallotus floribundus and M. miquelianus (Euphorbiaceae) and Dinophasma ruficornis mainly on Leea indica (Leeaceae) at the study site. Both specialists significantly preferred young leaves over old leaves of their respective host plants. In contrast, both generalists significantly preferred old leaves of the hosts of the specialist A. margaritatus . To reveal whether differential feeding choices were triggered by foliar chemistry, extracts (water, acetone, and hexane) of young leaves were applied to discs from old leaves and vice versa , and subjected to similar choice tests. For both Mallotus species, experimental results suggest that four chemical functions act in concert: (1) young leaves contain deterrents against generalists and (2) stimulants for specialists. Moreover, (3) old leaves contain deterrents against specialists and (4) stimulants for generalists. Deterrent compounds in young and old leaves, respectively, appeared in extracts using different solvents, suggesting the activity of multiple classes of secondary metabolites. Our study thus reveals that plant defences and herbivore offences are partly structured by leaf ontogeny and herbivore specialisation in a tropical plant-herbivore system.