Evolution Of Diet Breadth Research Articles

Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory

Plant-insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject to assessment in the same experimental context. Here, we address this knowledge gap using a recent host-range expansion onto alfalfa by the Melissa blue butterfly. Common garden rearing experiments and genomic data show that caterpillar performance depends on plant and insect genetic variation, with insect genetics contributing to performance earlier in development and plant genetics later. Our models of performance based on caterpillar genetics retained predictive power when applied to a second common garden. Much of the plant genetic effect could be explained by heritable variation in plant phytochemicals, especially saponins, peptides, and phosphatidyl cholines, providing a possible mechanistic understanding of variation in the species interaction. We find evidence of polygenic, mostly additive effects within and between species, with consistent effects of plant genotype on growth and development across multiple butterfly species. Our results inform theories of plant-insect coevolution and the evolution of diet breadth in herbivorous insects and other host-specific parasites.

A comprehensive phylogeny helps clarify the evolutionary history of host breadth and lure response in the Australian Dacini fruit flies (Diptera: Tephritidae)

The tribe Dacini (Diptera: Tephritidae) contains over 930 recognised species and has been widely studied due to the economic importance of some taxa, such as the Oriental fruit fly Bactrocera dorsalis. Despite the attention this group has received, very few phylogenetic reconstructions have comprehensively sampled taxa from a single biogeographic region, thereby limiting our capacity to address more targeted evolutionary questions. To study the evolution of diet breadth and male lure response, two key traits fundamental to understanding dacine diversity and the biology of pest taxa, we analysed 273 individuals representing 144 described species from Australia (80% continental coverage), the Pacific, and select close relatives from South-east Asia to estimate a dated molecular phylogenetic reconstruction of the Dacini. We utilised seven loci with a combined total of 4,332 nucleotides, to estimate both Bayesian and Maximum Likelihood phylogenies of the tribe. Consistent with other molecular phylogenies of the tribe, there was a high level of disagreement between the placement of species in the phylogeny and their current subgeneric and species-complex level taxonomies. The Australian fauna exhibit high levels of endemism, with radiations of both exclusively Australian clades, and clades that originate elsewhere (e.g. the Bactrocera dorsalis species group). Bidirectional movement of species has occurred between Papua New Guinea and Australia, with evidence for multiple incursions over evolutionary time. The Bactrocera aglaiae species group emerged sister to all other Bactrocera species examined. Divergence time estimates were ∼ 30 my younger than previously reported for this group, with the tribe diverging from its most recent common ancestor ∼ 43 mya. Ancestral trait reconstruction and tests for trait phylogenetic signal revealed a strong signal for the evolution of male lure response across the tree, with cue-lure/raspberry ketone lure response the ancestral trait. Methyl eugenol response has arisen on multiple, independent occasions. The evolution of host breadth exhibited a weaker signal; yet, basal groups were more likely to be host specialists. Both the evolution of lure response and host fruit use provide predictive information for the outbreak management of understudied pest fruit flies for which direct inference of these features may be lacking. Our results, which parallel those of earlier research into the closely-related African Dacus spp., demonstrate how geographically focussed taxon coverage allows Dacini phylogenetics to more explicitly test evolutionary hypotheses, thereby progressing our understanding of the evolution of this highly diverse and recently-radiated group of flies.

Plant pathogen-mediated rapid acclimation of a host-specialized aphid to a non-host plant.

Polyphagous aphids often consist of host‐specialized lineages, which have greater fitness on their native hosts than on others. The underlying causes are important for understanding of the evolution of diet breadth and host shift of aphids. The cotton‐melon aphid Aphis gossypii Glover is extremely polyphagous with many strict host‐specialized lineages. Whether and how the lineage specialized on the primary host hibiscus shifts to the secondary host cucumber remains elusive. We found that the hibiscus‐specialized lineage suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs on fresh cucumber leaves, and did not inflict any damage symptoms on cucumber plants. The poor performance did not improve with prolonged exposure to cucumber; however, it did significantly improve when the cucumber leaves were pre‐infected with a biotrophic phytopathogen Pseudoperonospora cubensis. More importantly, the hibiscus‐specialized lineage with two‐generation feeding experience on pre‐infected cucumber leaves performed as well as the cucumber‐specialized lineage did on fresh cucumber leaves, and inflicted typical damage symptoms on intact cucumber plants. Electrical penetration graph (EPG) indicated that the hibiscus‐specialized lineage did not ingest phloem sap from fresh cucumber leaves but succeeded in ingesting phloem sap from pre‐infected cucumber leaves, which explained the performance improvement of the hibiscus‐specialized lineage on pre‐infected cucumber leaves. This study revealed a new pathway for the hibiscus‐specialized lineage to quickly acclimate to cucumber under the assistance of the phytopathogen. We considered that the short feeding experience on pre‐infected cucumber may activate expression of effector genes that are related to specific host utilization. We suggest to identify host‐specific effectors by comparing proteomes or/and transcriptomes of the hibiscus‐specialized lineage before and after acclimating to cucumber.

What We Don't Know About Diet-Breadth Evolution in Herbivorous Insects

Half a million species of herbivorous insects have been described. Most of them are diet specialists, using only a few plant species as hosts. Biologists suspect that their specificity is key to their diversity. But why do herbivorous insects tend to be diet specialists? In this review, we catalog a broad range of explanations. We review the evidence for each and suggest lines of research to obtain the evidence we lack. We then draw attention to a second major question, namely how changes in diet breadth affect the rest of a species’ biology. In particular, we know little about how changes in diet breadth feed back on genetic architecture, the population genetic environment, and other aspects of a species’ ecology. Knowing more about how generalists and specialists differ should go a long way toward sorting out potential explanations of specificity, and yield a deeper understanding of herbivorous insect diversity.

The Life History of Chelymorpha alternans (Coleoptera: Chrysomelidae: Cassidinae) in Panamá

Here we describe an investigation of the life history characteristics, behavior, immature and adult morphologies of the Neotropical tortoise beetle Chelymorpha alternans (Boheman; Coleoptera: Chrysomelidae: Cassidinae) from the Republic of Panama. Developmental times and behavioral characteristics for individuals maintained under laboratory and field conditions are evaluated. Survival rates of individuals maintained under field and laboratory conditions are compared. A list of convolvulaceous host plants utilized by C. alternans is provided. Empirical studies investigating the biology of C. alternans are reviewed. This study contributes to our knowledge of quantitative and qualitative aspects of this lspecies' biology. These findings demonstrate that C. alternans is an organism that develops, behaves, and interacts with host plants, much as other tortoise beetles do. Rigorous, multi-year investigation of this ecologically representative species has produced a comparative life history description that expands our knowledge of general Cassidinae and Coleoptera biology. The natural history background, life history descriptions, diet breadth information, and literature review provided in this contribution make a compelling case for continued utilization of C. alternans as a representative tortoise beetle species for a variety of field and laboratory based studies in plant–insect interactions, chemical ecology, natural enemy ecology, and phenotypic trait and diet breadth evolution.

A Neutral Model for the Evolution of Diet Breadth.

Variation in diet breadth among organisms is a pervasive feature of the natural world that has resisted general explanation. In particular, trade-offs in the ability to use one resource at the expense of another have been expected but rarely detected. We explore a spatial model for the evolution of specialization, motivated by studies of plant-feeding insects. The model is neutral with respect to the causes and consequences of diet breadth: the number of hosts utilized is not constrained by trade-offs, and specialization or generalization does not confer a direct advantage with respect to the persistence of populations or the probability of diversification. We find that diet breadth evolves in ways that resemble reports from natural communities. Simulated communities are dominated by specialized species, with a predictable but less species-rich component of generalized taxa. These results raise the possibility that specialization might be a consequence of stochastic diversification dynamics acting on spatially segregated consumer-resource associations rather than a trait either favored or constrained directly by natural selection. Finally, our model generates hypotheses for global patterns of herbivore diet breadth, including a positive effect of host richness and a negative effect of evenness in host plant abundance on the number of specialized taxa.

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.

Evolving nutritional strategies in the presence of competition: a geometric agent-based model.

Access to nutrients is a key factor governing development, reproduction and ultimately fitness. Within social groups, contest-competition can fundamentally affect nutrient access, potentially leading to reproductive asymmetry among individuals. Previously, agent-based models have been combined with the Geometric Framework of nutrition to provide insight into how nutrition and social interactions affect one another. Here, we expand this modelling approach by incorporating evolutionary algorithms to explore how contest-competition over nutrient acquisition might affect the evolution of animal nutritional strategies. Specifically, we model tolerance of nutrient excesses and deficits when ingesting nutritionally imbalanced foods, which we term ‘nutritional latitude’; a higher degree of nutritional latitude constitutes a higher tolerance of nutritional excess and deficit. Our results indicate that a transition between two alternative strategies occurs at moderate to high levels of competition. When competition is low, individuals display a low level of nutritional latitude and regularly switch foods in search of an optimum. When food is scarce and contest-competition is intense, high nutritional latitude appears optimal, and individuals continue to consume an imbalanced food for longer periods before attempting to switch to an alternative. However, the relative balance of nutrients within available foods also strongly influences at what levels of competition, if any, transitions between these two strategies occur. Our models imply that competition combined with reproductive skew in social groups can play a role in the evolution of diet breadth. We discuss how the integration of agent-based, nutritional and evolutionary modelling may be applied in future studies to further understand the evolution of nutritional strategies across social and ecological contexts.

Ant association facilitates the evolution of diet breadth in a lycaenid butterfly

The role of mutualistic interactions in adaptive diversification has not been thoroughly examined. Lycaenid butterflies provide excellent systems for exploring mutualistic interactions, as more than half of this family is known to use ants as a resource in interactions that range from parasitism to mutualism. We investigate the hypothesis that protection from predators offered to caterpillars by ants might facilitate host-range evolution. Specifically, experiments with the butterfly Lycaeides melissa investigated the role of ant association in the use of a novel host, alfalfa, Medicago sativa, which is a sub-optimal host for larval development. Survival on alfalfa is increased by the presence of ants, thus supporting the hypothesis that interaction with ants might be important for host-range evolution. Using a demographic model to explore ecological conditions associated with host-range expansion in L. melissa, we conclude that the presence of ants might be an essential component for populations persisting on the novel, sub-optimal host.

Trophic ecology of New Zealand triplefin fishes (Family Tripterygiidae)

In many vertebrate radiations, food partitioning among closely related taxa is a key factor in both the maintenance of species diversity and the process of diversification. We compared diet composition and jaw morphology of 18 New Zealand triplefin species (F. Tripterygiidae) to examine whether species have diversified along a trophic axis. These fishes predominantly utilised small, mobile benthic invertebrates, and interspecific differences in diet composition appeared to be mainly attributable to habitat- or size-dependent feeding behaviour. Although there were differences in the relative size of the bones comprising the oral jaw apparatus between species, the majority showed an apparatus consistent with a relatively high velocity, low force jaw movement indicative of a diet of evasive prey. Phylogenetic comparative analyses showed that the evolution of jaw lever ratios and diet breadth was best explained by a non-directional model in which character changes have occurred randomly and independent of phylogeny. The mode of diet breadth evolution was gradual and the tempo has not accelerated or slowed down over time. The mode of evolution for the jaw lever ratios has been gradual for the opening but punctuated for the closing levers, suggesting that evolutionary changes have occurred rapidly for the latter trait. The tempo of trait evolution for the jaw opening levers has not accelerated or slowed down over time, while the tempo for the jaw closing levers has accelerated towards the tips of the tree, which is suggestive of species level adaptation. The lack of phylogenetic signal in diet breadth and jaw lever ratios appears most likely to be a correlated response to the marked habitat diversification in this group, and is thus the passive outcome of prey availability in species-specific habitat types. Overall, the trophic ecology of New Zealand’s triplefin fauna parallels the generalist strategy typical of the family worldwide, suggesting that trophic resource partitioning has not been an important factor in the evolution of these fishes.

The evolution of a pollen diet: Host choice and diet breadth ofAndrenabees (Hymenoptera: Andrenidae)

We investigate of two aspects of pollen diet of Andrena bees: the evolution of diet breadth within nearctic representatives of the genus, which includes both polylectic and oligolectic species; and host choice within an oligolectic clade of Andrena. We also evaluate phenology. Traits were mapped onto a molecular phylogeny to identify the ancestral character states. Overall, oligolecty appears to be the basal state within Andrena, and broader diets have evolved a number of times, suggesting that specialization is not a dead end. Within the oligolectic clade studied, host shifts occur predominantly between members of the same plant tribe, indicating a phylogenetic constraint to host-usage; however, shifts to other tribes are not uncommon, and may lead to adaptive radiation. Additionally, some lineages retain the ability to use pollen from an ancestral host-plant tribe. Finally, we find a correlation between using host plants in the family Asteraceae and fall emergence.

Host Plant Specialization Driven by Sexual Selection

We propose a new mechanism based on sexual selection to explain the evolution of diet breadth in insects. More specifically, we show that mate choice in females for certain diet-derived male pheromones can be exploited by maternal effect genes that preferentially place offspring on a specific host plant, resulting in specialization. Our analytical model also suggests that the process is more likely to occur with species that show male-congregating mating strategies, such as lekking and hilltopping. The model offers a new explanation for the similarity between the composition of male lepidopteran pheromones and the chemistry of their host plants and also suggests a novel mechanism of host plant shift. This is the first time that sexual selection has been proposed to drive host plant specialization and the first time that a mechanism with selection acting solely on the adult stage has been shown to be capable of determining larval feeding habits.

ECOLOGICAL AND EVOLUTIONARY DIVERSIFICATION OF THE SEED BEETLE GENUS STATOR (COLEOPTERA: CHRYSOMELIDAE: BRUCHINAE)

Ehrlich and Raven's (1964) hypothesis on coevolution has stimulated numerous phylogenetic studies that focus on the effects of plant defensive chemistry as the main ecological axis of phytophagous insect diversification. However, other ecological features affect host use and diet breadth and they may have very different consequences for insect evolution. In this paper, we present a phylogenetic study based on DNA sequences from mitochondrial and protein-coding genes of species in the seed beetle genus Stator, which collectively show considerable interspecific variation in host affiliation, diet breadth, and the dispersal stage of the seeds that they attack. We used comparative analyses to examine transitions in these three axes of resource use. We argue that these analyses show that diet breadth evolution is dependent upon colonizing novel hosts that are closely or distantly related to the ancestral host, and that oviposition substrate affects the evolution of host-plant affiliation, the evolution of dietary specialization, and the degree to which host plants are shared between species. The results of this study show that diversification is structured by interactions between different selective pressures and along multiple ecological axes.

Use of novel pollen species by specialist and generalist solitary bees (Hymenoptera: Megachilidae)

If trade-offs between flexibility to use a range of host species and efficiency on a limited set underlie the evolution of diet breadth, one resulting prediction is that specialists ought to be more restricted than generalists in their ability to use novel resource species. I used foraging tests and feeding trials to compare the ability of a generalist and a specialist solitary mason bee species to collect and develop on two pollen species that are not normally used in natural populations (novel pollens). Osmia lignaria (Hymenoptera: Megachilidae) is a generalist pollen feeder; O. californica, is more specialized. Adults of the specialist were more limited in use of novel hosts, but only in some contexts. Both bee species refused to collect one novel pollen. The specialist accepted a second novel pollen only when it was presented along with its normal pollen, whereas the generalist collected novel pollen whether presented alone or with normal pollen. Surprisingly, larvae of the specialist were more flexible than were generalists. The specialist grew well on mixtures of normal and novel pollen species, in some cases better than on its normal host alone. Larvae of the generalist grew more poorly on all diets containing novel pollens than on their normal host. Data on these two species of bees suggest that specialization by itself need not reduce flexibility on novel hosts. The findings also provide information about mechanisms of specialization in bees. Similar to some folivores, specific cues of the pollen host and the bee's interpretation of these contribute, along with foraging economics, to pollen choice by adults. The ability of the larvae to cope with specific components of one pollen species need not interfere with its ability to use others.

Specialists make faster decisions than generalists: experiments with aphids

Theoretical studies and a few recent experimental reports suggest that the evolution of diet breadth in herbivorous insects is constrained by a limited neural ability to efficiently process large amounts of information in short periods of time. This neural–constraints hypothesis predicts that generalist herbivores should make slower or poorer decisions than specialists when selecting plants, because generalists must discriminate and decide among stimuli from a wider variety of potential hosts. The present study compares the speed with which host–associated decisions are made in specialist versus generalist populations of the aphid Uroleucon ambrosiae . Populations of U. ambrosiae from eastern North America are highly specific to the host plant Ambrosia trifida (Asteraceae), whereas those from the American southwest also feed on a variety of other taxa from the Asteraceae. Experiments with winged (alate) and wingless (apterous) individuals showed that host–finding, host–selection, host–acceptance, host–sampling and host–settling were more efficiently performed by the eastern specialists. These very consistent results provide evidence that strongly supports the neural–constraints hypothesis.

Host-associated fitness trade-offs do not limit the evolution of diet breadth in the small milkweed bug Lygaeus kalmii (Hemiptera: Lygaeidae).

Theoretical models of evolution in a temporally variable environment predict that genotypes with low variance in fitness across generations will be favored. When host use varies temporally and fitness trade-offs exist among hosts, such that an increase in performance on one host results in a correlated decrease on the other, selection for low variance in fitness across generations will favor genotypes which are generalists. Before predictions such as this can be extended to natural herbivore populations, however, it is necessary to understand the extent to which performance trade-offs limit simultaneous adaptation to multiple hosts. The experiment reported here compares two populations of the common milkweed bug, Lygaeus kalmii (Hemiptera: Lygaeidae) which differ in patterns of host usage. One population is largely restricted to milkweed (Asclepias spp.) when milkweed seeds are available, but becomes a scavenger on a large assortment of available seeds when milkweed seeds are unavailable. The second population is restricted largely to dandelion (Taraxacum officinale), without access to milkweed. We examine these populations to test for host-associated genetic trade-offs between specialization on dandelion (Taraxacum) and two species of milkweed, Asclepias fascicularis, which is low in cardiac glycoside content, and A. speciosa, which is high in cardiac glycoside content. Despite the difference in patterns of host use of the two L. kalmii populations, the populations did not differ in their performance on any of the host plants. Within each population, bugs performed nearly as well on each host, except that bugs had significantly lower survivorship on dandelion than on either milkweed species. Trade-offs in performance among hosts were not present in either population: estimated genetic correlations across hosts were strongly positive. The inability of this study to detect host-associated fitness trade-offs is consistent with most published data on this topic.