Nonadaptive radiation: Pervasive diet specialization by drift in scale insects?

At least half of metazoan species are herbivorous insects. Why are they so diverse? Most herbivorous insects feed on few plant species, and adaptive host specialization is often invoked to explain their diversification. Nevertheless, it is possible that the narrow host ranges of many herbivorous insects are nonadaptive. Here, we test predictions of this hypothesis with comparative phylogenetic analyses of scale insects, a group for which there appear to be few host‐use trade‐offs that would select against polyphagy, and for which passive wind‐dispersal should make host specificity costly. We infer a strong positive relationship between host range and diversification rate, and a marked asymmetry in cladogenetic changes in diet breadth. These results are consonant with a system of pervasive nonadaptive host specialization in which small, drift‐ and extinction‐prone populations are frequently isolated from persistent and polyphagous source populations. They also contrast with the negative relationship between diet breadth and taxonomic diversification that has been estimated in butterflies, a disparity that likely stems from differences in the average costs and benefits of host specificity and generalism in scale insects versus butterflies. Our results indicate the potential for nonadaptive processes to be important to diet‐breadth evolution and taxonomic diversification across herbivorous insects.     

Patterns of host utilisation by herbivore assemblages of the genus Caloptilia (Lepidoptera; Gracillariidae) on congeneric maple tree (Acer) species

1. The pattern of host utilisation by congeneric Caloptilia caterpillars on 14 different species of Acer (maple) was investigated in temperate mixed forests of central Japan. A multi‐filtering model of host plant utilisation was proposed to address how phylogenetically related herbivore assemblages are constructed on phylogenetically related host plant species. 2. Two hypotheses were examined. The first questioned whether a negative relationship exists between the phylogenetic distance of plants from the most suitable host species and the abundance of herbivorous insects on the host. Regarding the second, it was investigated whether the assemblage dissimilarity of herbivorous insects among host plant species increases with increasing distance of plant phylogeny and traits. 3. Mantel and partial Mantel tests were used to measure the relationship between assemblage dissimilarity of Caloptilia species and the distance of plant phylogeny and leaf traits. 4. Both hypotheses were confirmed, clearly suggesting that the utilisation and suitability of hosts for Caloptilia caterpillars were strongly influenced by phylogenetic relatedness and leaf trait similarity among Acer species. This implies that phylogenetic distance is an integrated measure of phenotypic and ecological attributes of congeneric Acer species that can be used to explain specialisation and constraints of host utilisation of congeneric herbivore species even on a short evolutionary timescale.     

Simultaneous tests of the preference-performance and phylogenetic conservatism hypotheses: is either theory useful?

The preference-performance and phylogenetic conservatism hypotheses have been postulated to explain the mechanisms driving host-use patterns of phytophagous insects. The preference-performance hypothesis predicts that insects will use plants that provide higher offspring fitness, while the phylogenetic conservatism hypothesis predicts that insects will use phylogenetically closely related plants over more distantly related plants. Although some studies have supported these two hypotheses, others have not. Simultaneous tests of the two hypotheses on more than one species are lacking, and this limits comparative interpretation of previous studies. We undertook a comparative investigation to determine whether preference-performance and/or the phylogenetic conservatism hypothesis can explain host-use patterns of two phytophagous insects, the fruit flies Bactrocera cucumis and B. tryoni. Within a nested, plant phylogenetic framework, oviposition preference and offspring performance of the two fruit fly species were tested on fruits of plant species from across different plant families, from within a family and across cultivars within a species. The results show that both the preference-performance and the phylogenetic conservatism hypotheses can, depending on the host plant taxonomic level, explain host usage patterns in B. cucumis, while neither theory explained the host patterns seen in B. tryoni. In the light of increasing recognition of the complexity of host plant–herbivore relationships, and of ongoing studies which as often as not fail to find support for these theories as those that do, we discuss the limited value of either theory as a basis for future research.     

How do host plant use and seasonal life cycle relate to insect body size: A case study on European geometrid moths (Lepidoptera: Geometridae)

We used European geometrid moths (>630 species) as a model group to investigate how life history traits linked to larval host plant use (i.e., diet breadth and host-plant growth form) and seasonal life cycle (i.e., voltinism, overwintering stage and caterpillar phenology) are related to adult body size in holometabolous insect herbivores. To do so, we applied phylogenetic comparative methods to account for shared evolutionary history among herbivore species. We further categorized larval diet breadth based on the phylogenetic structure of utilized host plant genera. Our results indicate that species associated with woody plants are, on average, larger than herb feeders and increase in size with increasing diet breadth. Obligatorily univoltine species are larger than multivoltine species, and attain larger sizes when their larvae occur exclusively in the early season. Furthermore, the adult body size is significantly smaller in species that overwinter in the pupal stage compared to those that overwinter as eggs or caterpillars. In summary, our results indicate that the ecological niche of holometabolous insect herbivores is strongly interrelated with body size at maturity.     

Patterns of host plant utilization and diversification in the brush‐footed butterflies

Herbivorous insects represent one of the most successful animal radiations known. They occupy a wide range of niches, feed on a great variety of plants, and are species rich; yet the factors that influence their diversification are poorly understood. Host breadth is often cited as a major factor influencing diversification, and, according to the Oscillation Hypothesis, shifts from generalist to specialist feeding states increase the diversification rate for a clade. We explored the relationship between host breadth and diversification within the Nymphalidae (Lepidoptera) and explicitly tested predictions of the Oscillation Hypothesis. We found strong evidence of diversification rate heterogeneity, but no difference in host breadth between clades with a higher diversification rate compared to their sisters. We also found some clades exhibited phylogenetic nonindependence in host breadth and these clades had lower host plant turnover than expected by chance, suggesting host breadth is evolutionarily constrained. Finally, we found that transitions among host breadth categories varied, but the likelihood of reductions in host breadth was greater than that of increases. Our results indicate host breadth is decoupled from diversification rate within the Nymphalidae, and that constraints on diet breadth might play an important role in the evolution of herbivorous insects.     

When do herbivorous insects compete? A phylogenetic meta‐analysis

When herbivorous insects interact, they can increase or decrease each other's fitness. As it stands, we know little of what causes this variation. Classic competition theory predicts that competition will increase with niche overlap and population density. And classic hypotheses of herbivorous insect diversification predict that diet specialists will be superior competitors to generalists. Here, we test these predictions using phylogenetic meta‐analysis. We estimate the effects of diet breadth, population density and proxies of niche overlap: phylogenetic relatedness, physical proximity and feeding‐guild membership. As predicted, we find that competition between herbivorous insects increases with population density as well as phylogenetic and physical proximity. Contrary to predictions, competition tends to be stronger between than within feeding guilds and affects specialists as much as generalists. This is the first statistical evidence that niche overlap increases competition between herbivorous insects. However, niche overlap is not everything; complex feeding guild effects indicate important indirect interactions.     

The relationship between diet breadth and geographic range size in the butterfly subfamily Nymphalinae--a study of global scale

The "oscillation hypothesis" has been proposed as a general explanation for the exceptional diversification of herbivorous insect species. The hypothesis states that speciation rates are elevated through repeated correlated changes--oscillations--in degree of host plant specificity and geographic range. The aim of this study is to test one of the predictions from the oscillation hypothesis: a positive correlation between diet breadth (number of host plants used) and geographic range size, using the globally distributed butterfly subfamily Nymphalinae. Data on diet breadth and global geographic range were collected for 182 Nymphalinae butterflies species and the size of the geographic range was measured using a GIS. We tested both diet breadth and geographic range size for phylogenetic signal to see if species are independent of each other with respect to these characters. As this test gave inconclusive results, data was analysed both using cross-species comparisons and taking phylogeny into account using generalised estimating equations as applied in the APE package in R. Irrespective of which method was used, we found a significant positive correlation between diet breadth and geographic range size. These results are consistent for two different measures of diet breadth and removal of outliers. We conclude that the global range sizes of Nymphalinae butterflies are correlated to diet breadth. That is, butterflies that feed on a large number of host plants tend to have larger geographic ranges than do butterflies that feed on fewer plants. These results lend support for an important step in the oscillation hypothesis of plant-driven diversification, in that it can provide the necessary fuel for future population fragmentation and speciation.     

Variation of butterfly diet breadth in relation to host-plant predictability: results from two faunas

Host‐plant data for North American and Australian butterflies were used to test the hypothesis that larval diet breadth increases with decreasing resource predictability (where the latter was estimated by host‐plant growth‐form/duration). For each region in turn we compared the diet breadths of butterflies which utilise herbaceous host‐plants with those of species having woody hosts. For North America alone we also compared the diet breadths of species having annual hosts with those utilising perennial hosts, and the diets of species having herbaceous‐annual hosts with those using woody‐perennial hosts. Studies of diet breadth may be biased by the host taxonomic level which contributes most to the diet index used. For example, the results of analyses which employ indices based on numbers of families of hosts utilised may differ from those using indices based on counts of host species or genera. To investigate this potential problem we performed cross‐species analyses where diet breadth was defined in turn as the number of host species, genera, or families eaten. We found that using different taxonomic levels did give inconsistent results. To avoid this we employed phylogenetic diet breadth indices in comparative analyses of Independent Contrasts. The former incorporate information from the whole of the host‐plant phylogeny, whilst the comparative method eliminates any confounding effects of butterfly phylogeny. The results indicated that there is a phylogenetic component to butterfly diet breadth. They also largely differed from those of the cross‐species investigations, although there were similarities (i.e. results differed between regions and varied according to whether the whole fauna or just endemics were investigated). Our results suggested that in both regions, non‐endemics which feed on herbaceous plants have wider diet breadths than non‐endemics which utilise woody hosts. However, we found no consistent evidence that the diet breadths of endemics increase with decreasing resource predictability (as estimated here).     

The Evolution of Body Size,Antennal Size and Host Use in Parasitoid Wasps (Hymenoptera: Chalcidoidea): A Phylogenetic Comparative Analysis

Chalcidoid wasps represent one of the most speciose superfamilies of animals known, with ca. 23,000 species described of which many are parasitoids. They are extremely diverse in body size, morphology and, among the parasitoids, insect hosts. Parasitic chalcidoids utilise a range of behavioural adaptations to facilitate exploitation of their diverse insect hosts, but how host use might influence the evolution of body size and morphology is not known in this group. We used a phylogenetic comparative analysis of 126 chalcidoid species to examine whether body size and antennal size showed evolutionary correlations with aspects of host use, including host breadth (specificity), host identity (orders of insects parasitized) and number of plant associates. Both morphological features and identity of exploited host orders show strong phylogenetic signal, but host breadth does not. Larger body size in these wasps was weakly associated with few plant genera, and with more specialised host use, and chalcidoid wasps that parasitize coleopteran hosts tend to be larger. Intriguingly, chalcidoid wasps that parasitize hemipteran hosts are both smaller in size in the case of those parasitizing the suborder Sternorrhyncha and have relatively larger antennae, particularly in those that parasitize other hemipteran suborders. These results suggest there are adaptations in chalcidoid wasps that are specifically associated with host detection and exploitation.     

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

The present study is the first to consider human and nonhuman consumers together to reveal several general patterns of plant utilization. We provide evidence that at a global scale, plant apparency and phylogenetic isolation can be important predictors of plant utilization and consumer diversity. Using the number of species or genera or the distribution area of each plant family as the island “area” and the minimum phylogenetic distance to common plant families as the island “distance”, we fitted presence–area relationships and presence–distance relationships with a binomial GLM (generalized linear model) with a logit link. The presence–absence of consumers among each plant family strongly depended on plant apparency (family size and distribution area); the diversity of consumers increased with plant apparency but decreased with phylogenetic isolation. When consumers extended their host breadth, unapparent plants became more likely to be used. Common uses occurred more often on common plants and their relatives, showing higher host phylogenetic clustering than uncommon uses. On the contrary, highly specialized uses might be related to the rarity of plant chemicals and were therefore very species‐specific. In summary, our results provide a global illustration of plant–consumer combinations and reveal several general patterns of plant utilization across humans, insects and microbes. First, plant apparency and plant phylogenetic isolation generally govern plant utilization value, with uncommon and isolated plants suffering fewer parasites. Second, extension of the breadth of utilized hosts helps explain the presence of consumers on unapparent plants. Finally, the phylogenetic clustering structure of host plants is different between common uses and uncommon uses. The strength of such consistent plant utilization patterns across a diverse set of usage types suggests that the persistence and accumulation of consumer diversity and use value for plant species are determined by similar ecological and evolutionary processes.     

Use of exotic hosts by Lepidoptera: widespread species colonize more novel hosts

The study of host shifts by herbivorous insects has played an important role in evolutionary biology, contributing to research in coevolution, ecological speciation, and adaptive radiation. As invasive plants become more abundant in many ecosystems, the potential for exotic host use by native insects increases. Graves and Shapiro (2003) have documented exotic host use by 34% of Californian butterflies, suggesting that the plants and butterflies of California might be an important model system for the colonization and utilization of novel resources. In this study, we analyze relationships among geographic range, native diet breadth, and the use of exotic hosts by Californian butterflies and skippers (Lepidoptera). Geographic range and, to a lesser extent, native diet breadth are significant predictors of exotic host use, with positive relationships found both before and after phylogenetic correction. These results give insight into the process of insect host range evolution, as geographically widespread generalists have an apparently greater tendency to use novel, exotic hosts than geographically constrained specialists. Increasing occurrences of exotic host use are expected and those species not capable of shifting to nonnative hosts are likely to have higher vulnerability to extirpation and extinction in the future.     

Proportion of exotics and relatedness of host species mediate the positive effect of plant richness on the species richness of fruit flies

1. All else being equal, the greater the local species richness of plants, the greater the number of associated herbivore species. Because most herbivore insects feed on a subset of closely related plant species, plant phylogenetic diversity is expected to play a key role in determining the number of herbivore species. What is not well known, however, is how an increase in the species richness of exotic plants affects the species richness of herbivores. 2. In this study, we used plant–fruit fly interactions to investigate the influence of the proportion and species richness of exotic host plants on the species richness of herbivorous insects. We also tested whether the phylogenetic diversity of host plants increases when the number of exotic plant species increases. 3. We found that the species richness of fruit flies is more accurately predicted by the richness of native host plants than by total plant species richness (including both native and exotic species). The proportion of exotic host species and the phylogenetic diversity of host plants had negative and positive effects, respectively, on the species richness of fruit flies. 4. Our findings suggest that a positive effect of plant richness on herbivore richness occurs only when an increase in plant diversity involves plant species with which native herbivores share some evolutionary history.     

Using biological traits to explain ladybird distribution patterns

Aim  Determining to what extent differing distribution patterns are governed by species’ life‐history and resource‐use traits may lead to an improved understanding of the impacts of environmental change on biodiversity. We investigated the extent to which traits can explain distribution patterns in the ladybird fauna (Coleoptera: Coccinellidae) of Great Britain. Location  The British mainland and inshore islands (Anglesey, the Isle of Wight and the Inner Hebrides). Methods  The distributions of 26 ladybird species resident in Britain were characterized in terms of their range size (from 2661 10‐km grid squares across Britain) and proportional range fill (at 10‐ and 50‐km scales). These were assessed relative to five traits (body length, elytral colour pattern polymorphism, voltinism, habitat specificity and diet breadth). The role of phylogenetic autocorrelation was examined by comparing the results of phylogenetic and generalized least‐squares regressions. Results  Diet breadth was the only trait correlated with range size: species with broad diets had larger range sizes than dietary specialists. Range fill was sensitive to recording intensity (a per‐species measure of the mean number of records across occupied squares); models including both recording intensity and range size provided more explanatory power than models incorporating ecological traits alone. Main conclusions  Habitat specificity is often invoked to explain the distribution patterns of species, but here we found diet breadth to be the only ecological correlate of both range fill and range size. This highlights the importance of understanding predator–prey interactions when attempting to explain the distribution patterns of predatory species. Our results suggest that the diet breadth of predatory species is a better correlate of range size and fill than other measures, such as habitat specificity.     

Use of an exotic host plant affects mate choice in an insect herbivore

The colonization of exotic plants by herbivorous insects has provided opportunities for investigating causes and consequences of the evolution of niche breadth. The butterfly Lycaeides melissa utilizes exotic alfalfa, Medicago sativa, which is a relatively poor larval resource, and previous studies have found that caterpillars that consume M. sativa develop into smaller and less fecund adults. Here we investigate the effect of smaller female body size on male mate preference, a previously unexplored consequence of novel host use. Smaller females, which developed on the exotic host, were less likely to be visited by males. This result was confirmed with a second set of choice tests involving females reared on a single plant species, thus ruling out host-specific confounding factors. We suggest that an effect on mate choice be considered part of the complex suite of factors determining persistence of herbivorous insects following colonization of new habitats or resources.     

Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses

Evolutionary biologists have often assumed that ecological generalism comes at the expense of less intense exploitation of specific resources and that this trade-off will promote the evolution of ecologically specialized daughter species. Using a phylogenetic comparative approach with butterflies as a model system, we test hypotheses that incorporate changes in niche breadth and location into explanations of the taxonomic diversification of insect herbivores. Specifically, we compare the oscillation hypothesis, where speciation is driven by host-plant generalists giving rise to specialist daughter species, to the musical chairs hypothesis, where speciation is driven by host-plant switching, without changes in niche breadth. Contrary to the predictions of the oscillation hypothesis, we recover a negative relationship between host-plant breadth and diversification rate and find that changes in host breadth are seldom coupled to speciation events. By contrast, we present evidence for a positive relationship between rates of host switching and butterfly diversification, consonant with the musical chairs hypothesis. These results suggest that the costs of trophic generalism in plant-feeding insects may have been overvalued and that transitions from generalists to ecological specialists may not be an important driver of speciation in general.     

Similarity and specialization of the larval versus adult diet of European butterflies and moths

Many herbivorous insects feed on plant tissues as larvae but use other resources as adults. Adult nectar feeding is an important component of the diet of many adult herbivores, but few studies have compared adult and larval feeding for broad groups of insects. We compiled a data set of larval host use and adult nectar sources for 995 butterfly and moth species (Lepidoptera) in central Europe. Using a phylogenetic generalized least squares approach, we found that those Lepidoptera that fed on a wide range of plant species as larvae were also nectar feeding on a wide range of plant species as adults. Lepidoptera that lack functional mouthparts as adults used more plant species as larval hosts, on average, than did Lepidoptera with adult mouthparts. We found that 54% of Lepidoptera include their larval host as a nectar source. By creating null models that described the similarity between larval and adult nectar sources, we furthermore showed that Lepidoptera nectar feed on their larval host more than would be expected if they fed at random on available nectar sources. Despite nutritional differences between plant tissue and nectar, we show that there are similarities between adult and larval feeding in Lepidoptera. This suggests that either behavioral or digestive constraints are retained throughout the life cycle of holometabolous herbivores, which affects host breadth and identity.     

Adaptive significance of food income in European snakes: body size is related to prey energetics

Feeding strategies and diet patterns have been extensively investigated in vertebrates and, more specifically, in snakes. Although it has been hypothesized that prey species may differ in terms of energy content, almost no theoretical or practical study has been carried out to determine actual nutritional values of the common prey types of wild snakes. Our model taxa were a selection of widely distributed and well known European snake species, which have all been studied in depth: approximately 76% of their diet is composed of mammals, reptiles, and insects. We therefore selected a single model species for each of these categories and proceeded with the analyses. Nutritional values were determined using a standard procedure: lizards and mice were richer in proteins than insects (crickets); insects and mice were richer in lipids than lizards, and mice and crickets have a higher energy content than lizards; lizards were rich in ashes. We then applied our experimental results to a selected sample of European terrestrial snakes (11 populations, ten species, seven genera, two families) characterized by different body size (50–160 cm total length) and reproductive strategies (oviparous versus viviparous), aiming to correlate these parameters with patterns of energy income. A direct relationship was found between body mass/body length ratio (BCI, body condition index) and meal energetics: the higher the BCI, the higher was the metabolic requirement, whereas BCI was independent of species or of reproductive system effect. Large‐sized snakes thus need a highly diversified and more energy‐rich diet than smaller snakes, supporting previous hypotheses. The simple applicability of this method could be of valuable support in further comparative research work, reducing experimental costs and stimulating further ecological, behavioural, and, possibly, phylogenetic comparisons. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 307–317.     

Do diet and taxonomy influence insect gut bacterial communities?

Many insects contain diverse gut microbial communities. While several studies have focused on a single or small group of species, comparative studies of phylogenetically diverse hosts can illuminate general patterns of host–microbiota associations. In this study, we tested the hypotheses that (i) host diet and (ii) host taxonomy structure intestinal bacterial community composition among insects. We used published 16S rRNA gene sequence data for 58 insect species in addition to four beetle species sampled from the Sevilleta National Wildlife Refuge to test these hypotheses. Overall, gut bacterial species richness in these insects was low. Decaying wood xylophagous insects harboured the richest bacterial gut flora (102.8 species level operational taxonomic units (OTUs)/sample ± 71.7, 11.8 ± 5.9 phylogenetic diversity (PD)/sample), while bees and wasps harboured the least rich bacterial communities (11.0 species level OTUs/sample ± 5.4, 2.6 ± 0.8 PD/sample). We found evidence to support our hypotheses that host diet and taxonomy structure insect gut bacterial communities (P < 0.001 for both). However, while host taxonomy was important in hymenopteran and termite gut community structure, diet was an important community structuring factor particularly for insect hosts that ingest lignocellulose‐derived substances. Our analysis provides a baseline comparison of insect gut bacterial communities from which to test further hypotheses concerning proximate and ultimate causes of these associations.     

Does host‐plant diversity explain species richness in insects? A test using Coccidae (Hemiptera)

1. The megadiverse herbivores and their host plants are a major component of biodiversity, and their interactions have been hypothesised to drive the diversification of both. 2. If plant diversity influences the diversity of insects, there is an expectation that insect species richness will be strongly correlated with host‐plant species richness. This should be observable at two levels (i) more diverse host‐plant groups should harbour more species of insects, and (ii) the species richness of a group of insects should correlate with the richness of the host groups it uses. However, such a correlation is also consistent with a hypothesis of random host use, in which insects encounter and use hosts in proportion to the diversity of host plants. Neither of these expectations has been widely tested. 3. These expectations were tested using data from a species‐rich group of insects – the Coccidae (Hemiptera). 4. Significant positive correlations were found between the species richness of coccid clades (genera) and the species richness of the host‐plant family or families upon which the clades occur. On a global scale, more closely related plant families have more similar communities of coccid genera but the correlation is weak. 5. Random host use could not be rejected for many coccids but randomisation tests and similarity of coccid communities on closely related plant families show that there is non‐random host use in some taxa. Overall, our results support the idea that plant diversity is a driver of species richness of herbivorous insects, probably via escape‐and‐radiate or oscillation‐type processes.     

Ecological correlates of body size in gamasid mites parasitic on small mammals: abundance and niche breadth

We studied ecological correlates of body size (abundance and niche breadth) in gamasid mites parasitic on small mammals in 28 regions of the Palearctic. We predicted that smaller species would be characterized by higher abundance than larger species, all else (e.g. host species) being equal. We also predicted that host specificity of mites would decrease (that is, number of host species they use would increase) with an increase in their body size. We focused on mites collected from host bodies that include a) species that feed solely on host’s blood (obligate exclusive haematophages), b) species that feed on both host’s blood and small arthropods (obligate non‐exclusive haematophages), and c) facultative haematophages. We expected that the relationship between body size and abundance and/or host specificity would be more pronounced in obligate exclusively haematophagous mites than for obligate non‐exclusively and facultative haematophagous mites. Across all mite species across regions, mean abundance correlated negatively with body size. The same was true for obligate haematophagous species, but not for facultative haematophages. When mite communities on the same host in a location were considered, the negative body mass–abundance relationship was found in only 3 of 44 communities. Nevertheless, a meta‐analytic (across host species) estimate of the slope of this relationship appeared to be significantly negative. No significant relationship between mite body size and host specificity was found in the analyses across all mite species as well as in obligate exclusive or obligate non‐exclusive haematophages. However, the number of hosts used by facultative haematophagous mites decreased significantly with an increase in their body size. We explain the relationships between morphological (body size) and ecological (abundance and niche breadth) properties of ectoparasites by their interactions with hosts or physical environment.