A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins.

Butterflies are a diverse and charismatic insect group that are thought to have evolved with plants and dispersed throughout the world in response to key geological events. However, these hypotheses have not been extensively tested because a comprehensive phylogenetic framework and datasets for butterfly larval hosts and global distributions are lacking. We sequenced 391 genes from nearly 2,300 butterfly species, sampled from 90 countries and 28 specimen collections, to reconstruct a new phylogenomic tree of butterflies representing 92% of all genera. Our phylogeny has strong support for nearly all nodes and demonstrates that at least 36 butterfly tribes require reclassification. Divergence time analyses imply an origin ~100 million years ago for butterflies and indicate that all but one family were present before the K/Pg extinction event. We aggregated larval host datasets and global distribution records and found that butterflies are likely to have first fed on Fabaceae and originated in what is now the Americas. Soon after the Cretaceous Thermal Maximum, butterflies crossed Beringia and diversified in the Palaeotropics. Our results also reveal that most butterfly species are specialists that feed on only one larval host plant family. However, generalist butterflies that consume two or more plant families usually feed on closely related plants.

Niche Specificity, Polygeny, and Pleiotropy in Herbivorous Insects.

AbstractWhat causes host use specificity in herbivorous insects? Population genetic models predict specialization when habitat preference can evolve and there is antagonistic pleiotropy at a performance-affecting locus. But empirically for herbivorous insects, host use performance is governed by many genetic loci, and antagonistic pleiotropy seems to be rare. Here, we use individual-based quantitative genetic simulation models to investigate the role of pleiotropy in the evolution of sympatric host use specialization when performance and preference are quantitative traits. We look first at pleiotropies affecting only host use performance. We find that when the host environment changes slowly, the evolution of host use specialization requires levels of antagonistic pleiotropy much higher than what has been observed in nature. On the other hand, with rapid environmental change or pronounced asymmetries in productivity across host species, the evolution of host use specialization readily occurs without pleiotropy. When pleiotropies affect preference as well as performance, even with slow environmental change and host species of equal productivity, we observe fluctuations in host use breadth, with mean specificity increasing with the pervasiveness of antagonistic pleiotropy. Thus, our simulations show that pleiotropy is not necessary for specialization, although it can be sufficient, provided it is extensive or multifarious.

Aphid male wing polymorphisms are transient and have evolved repeatedly.

Polymorphic phenotypes have long been used to examine the maintenance of genetic variation within and between species. Most studies have focused on persistent polymorphisms, which are retained across species boundaries, and their positive effects on speciation rates. Far less is known about the macroevolutionary impacts of more transient polymorphisms, which are also common. Here we investigated male wing polymorphisms in aphids. We estimated the phylogenetic history of wing states across species, along with several other traits that could affect wing evolution. We found that male wing polymorphisms are transient: they are found in only ~4% of extant species, but have likely evolved repeatedly across the phylogeny. We reason that the repeated evolution of transient polymorphisms might be facilitated by the existence of the asexual female wing plasticity, which is common across aphids, and would maintain the wing development program even in species with wingless males. We also discovered that male wingedness correlates positively with host plant alternation and host plant breadth, and that winged morphs and wing polymorphisms may be associated with higher speciation rates. Our results provide new evolutionary insights into this well-studied group and suggest that even transient polymorphisms may impact species diversification rates.

Delaying quantitative resistance to pesticides and antibiotics.

How can we best vary the application of pesticides and antibiotics to delay resistance evolution? Previous theoretical comparisons of deployment strategies have focused on qualitative resistance traits and have mostly assumed that resistance alleles are already present in a population. But many real resistance traits are quantitative, and the evolution of resistant genotypes in the field may depend on de novo mutation and recombination. Here, I use an individual-based, forward-time, quantitative-genetic simulation model to investigate the evolution of quantitative resistance. I evaluate the performance of four application strategies for delaying resistance evolution, to wit, the (1) sequential, (2) mosaic, (3) periodic, and (4) combined strategies. I find that which strategy is best depends on initial efficacy. When at the onset, xenobiotics completely prevent reproduction in treated demes, a combined strategy is best. On the other hand, when populations are partially resistant, the combined strategy is inferior to mosaic and periodic strategies, especially when resistance alleles are antagonistically pleiotropic. Thus, the optimal application strategy for managing against the rise of quantitative resistance depends on pleiotropy and whether or not partial resistance is already present in a population. This result appears robust to variation in pest reproductive mode and migration rate, direct fitness costs for resistant phenotypes, and the extent of refugial habitats.

Geographic isolation drives speciation in Nearctic aphids.

Across herbivorous insect clades, species richness and host-use diversity tend to positively covary. This could be because host-use divergence drives speciation, or because it raises the ecological limits on species richness. To evaluate these hypotheses, we performed phylogenetic path model analyses of the species diversity of Nearctic aphids. Here, we show that variation in the species richness of aphid clades is caused mainly by host-use divergence, whereas variation in speciation rates is caused more by divergence in non-host-related niche variables. Aphid speciation is affected by both the evolution of host and non-host-related niche components, but the former is largely caused by the latter. Thus, our analyses suggest that host-use divergence can both raise the ecological limits on species richness and drive speciation, although in the latter case, host-use divergence tends to be a step along the causal path leading from non-host-related niche evolution to speciation.

Insect-plant relationships predict the speed of insecticide adaptation.

Herbivorous insects must circumvent the chemical defenses of their host plants and, in cropping systems, must also circumvent synthetic insecticides. The pre-adaptation hypothesis posits that when herbivorous insects evolve resistance to insecticides, they co-opt adaptations against host plant defenses. Despite its intuitive appeal, few predictions of this hypothesis have been tested systematically. Here, with survival analysis of more than 17,000 herbivore-insecticide interactions, we show that resistance evolution tends to be faster when herbivorous insect diets are broad (but not too broad) and when insecticides and plant defensive chemicals are similar (but not too similar). These general relations suggest a complex interplay between macro-evolutionary contingencies and contemporary population genetic processes, and provide a predictive framework to forecast which pest species are most likely to develop resistance to particular insecticide chemistries.

Nonadaptive host-use specificity in tropical armored scale insects.

Most herbivorous insects are diet specialists in spite of the apparent advantages of being a generalist. This conundrum might be explained by fitness trade-offs on alternative host plants, yet the evidence of such trade-offs has been elusive. Another hypothesis is that specialization is nonadaptive, evolving through neutral population-genetic processes and within the bounds of historical constraints. Here, we report on a striking lack of evidence for the adaptiveness of specificity in tropical canopy communities of armored scale insects. We find evidence of pervasive diet specialization, and find that host use is phylogenetically conservative, but also find that more-specialized species occur on fewer of their potential hosts than do less-specialized species, and are no more abundant where they do occur. Of course local communities might not reflect regional diversity patterns. But based on our samples, comprising hundreds of species of hosts and armored scale insects at two widely separated sites, more-specialized species do not appear to outperform more generalist species.

Do major host shifts spark diversification in butterflies?

The Escape and Radiate Hypothesis posits that herbivorous insects and their host plants diversify through antagonistic coevolutionary adaptive radiation. For more than 50 years, it has inspired predictions about herbivorous insect macro-evolution, but only recently have the resources begun to fall into place for rigorous testing of those predictions. Here, with comparative phylogenetic analyses of nymphalid butterflies, we test two of these predictions: that major host switches tend to increase species diversification and that such increases will be proportional to the scope of ecological opportunity afforded by a particular novel host association. We find that by and large the effect of major host-use changes on butterfly diversity is the opposite of what was predicted; although it appears that the evolution of a few novel host associations can cause short-term bursts of speciation, in general, major changes in host use tend to be linked to significant long-term decreases in butterfly species richness.

Biting Rates and Onchocerca Infectivity Status of Black Flies from the Simulium damnosum Complex (Diptera: Simuliidae) in Osun State, Nigeria.

The Simulium damnosum Theobald complex transmits Onchocerca volvulus Leuckart (Spirurida: Onchocercidae), the causative agent of onchocerciasis. Recent evidence suggests that control efforts have strongly suppressed parasite populations, but vector surveillance is needed in parts of Africa where the disease remains endemic. Here, studies on biting rates and infectivity status of suspected vector species were conducted in three onchocerciasis-endemic areas, namely Iwo, Ede, and Obokun, in Osun State, Nigeria. A total of 3,035 black flies were collected between October 2014 and September 2016, and examined for parity and parasites using standard methods. A separate collection of 2,000 black flies was pool-screened for infectivity using polymerase chain reaction (PCR) amplification of the O-150 marker. Results showed that parous flies were significantly less common than nulliparous flies with overall parous rates of 8.02% in Iwo and 35.38% in Ede at the end of the study period. Obokun had a parous rate of 22.22% obtained in the first year only. None of the dissected parous flies were infected with O. volvulus and PCR assays showed no amplification of O-150 O. volvulus-specific repeats in head and body pools. However, annual biting rates exceeded the World Health Organization threshold of 1,000 bites/person/yr. Thus it appears that, with such high rates of biting, even low levels of vector infection can sustain onchocerciasis in African communities.

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.

A revision of Lachnodius Maskell (Hemiptera, Coccomorpha, Eriococcidae).

Lachnodius Maskell is a genus of three named species that are part of an Australian radiation of felt scale insects that induce galls on Eucalyptus and Corymbia (Myrtaceae). A female's gall usually consists of an open-top pit in swollen plant tissue. Depending on the species, galls can occur on a host's leaves, buds, stems, or trunk. Here, we redescribe the named species: L.eucalypti (Maskell), L.hirsutus (Froggatt) and L.lectularius (Maskell), and describe seven new species: L.brimblecombei Beardsley, Gullan & Hardy, sp. n., L.froggatti Beardsley, Gullan & Hardy, sp. n., L.maculosus Beardsley, Gullan & Hardy, sp. n., L.melliodorae Beardsley, Gullan & Hardy, sp. n., L.newi Beardsley, Gullan & Hardy, sp. n., L.parathrix Beardsley, Gullan & Hardy, sp. n., L.sealakeensis Gullan & Hardy, sp. n. Descriptions are based primarily on adult females, but for some species short diagnoses of nymphal stages also are provided. The taxonomic history of Lachnodius is reviewed, with notes on their biology and ecology. A key to species based on the morphology of adult females is provided, and lectotypes are designated for Dactylopiuseucalypti Maskell and Lachnodiuslectularius Maskell.

Phylogenomics and the evolution of hemipteroid insects.

Hemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previous phylogenetic analyses have not consistently resolved the relationships among major hemipteroid lineages. We provide maximum likelihood-based phylogenomic analyses of a taxonomically comprehensive dataset comprising sequences of 2,395 single-copy, protein-coding genes for 193 samples of hemipteroid insects and outgroups. These analyses yield a well-supported phylogeny for hemipteroid insects. Monophyly of each of the three hemipteroid orders (Psocodea, Thysanoptera, and Hemiptera) is strongly supported, as are most relationships among suborders and families. Thysanoptera (thrips) is strongly supported as sister to Hemiptera. However, as in a recent large-scale analysis sampling all insect orders, trees from our data matrices support Psocodea (bark lice and parasitic lice) as the sister group to the holometabolous insects (those with complete metamorphosis). In contrast, four-cluster likelihood mapping of these data does not support this result. A molecular dating analysis using 23 fossil calibration points suggests hemipteroid insects began diversifying before the Carboniferous, over 365 million years ago. We also explore implications for understanding the timing of diversification, the evolution of morphological traits, and the evolution of mitochondrial genome organization. These results provide a phylogenetic framework for future studies of the group.

Doubling the known endemic species diversity of New Caledonian armored scale insects (Hemiptera, Diaspididae).

Fourteen species of armored scale insects are known only from New Caledonia. Here, the adult female of fourteen more are described: Agrophaspisansevatae sp. n., Aonidiamontikoghis sp. n. , Aonidiapauca sp. n., Fernaldannawhita sp. n., Furcaspiscostulariae sp. n., Greeniellacasuarinae sp. n., Greenielladacrydiae sp. n., Lepidosaphesmonticola sp. n., Leptaspispege gen. et sp. n., Leucaspismontikoghis sp. n., Melanaspisnothofagi sp. n., Neomorganianothofagi sp. n., Pseudaonidiadugdali sp. n., and Pseudaonidiayateensis sp. n. We note that the diversity of New Caledonian armored scale insects appears to have resulted more from trans-oceanic dispersal than in situ speciation.

Does a plant-eating insect's diet govern the evolution of insecticide resistance? Comparative tests of the pre-adaptation hypothesis.

According to the pre-adaptation hypothesis, the evolution of insecticide resistance in plant-eating insects co-opts adaptations that initially evolved during chemical warfare with their host plants. Here, we used comparative statistics to test two predictions of this hypothesis: (i) Insects with more diverse diets should evolve resistance to more diverse insecticides. (ii) Feeding on host plants with strong or diverse qualitative chemical defenses should prime an insect lineage to evolve insecticide resistance. Both predictions are supported by our tests. What makes this especially noteworthy is that differences in the diets of plant-eating insect species are typically ignored by the population genetic models we use to make predictions about insecticide resistance evolution. Those models surely capture some of the differences between host-use generalists and specialists, for example, differences in population size and migration rates into treated fields, but they miss other potentially important differences, for example, differences in metabolic diversity and gene expression plasticity. Ignoring these differences could be costly.

Five new species of the armored scale genus Andaspis MacGillivray (Hemiptera, Coccomorpha, Diaspididae) from New Caledonia.

New Caledonia is home to many endemic species of plants and animals. Here, we improve our grasp on that biota by describing five new species of armored scale insects in the genus Andaspis: Andaspis brevicornutasp. n, A. conicasp. n., A. nothofagisp. n., A. novaecaledoniaesp. n., and A. ornatasp. n. Each is known exclusively from collections on southern beeches (Nothofagus spp.) in New Caledonia. A key to the species of Andaspis of New Caledonia is provided.

Do plant-eating insect lineages pass through phases of host-use generalism during speciation and host switching? Phylogenetic evidence.

The Oscillation Hypothesis posits that plant-eating insect diversity is generated by cycles of diet breadth expansion and contraction. Although at any given time most plant-eating insect species are host specialists, host-use evolution and speciation tend to entail a phase of generalism. The main evidence for this comes from comparative phylogenetic studies, but with mixed support. Here, I review and add to this evidence. I show that some of the original work that inspired the Oscillation Hypothesis is flawed in a way that leads to spurious inferences about trends in the evolution of diet diversity. And I present a new analysis which fails to support its predictions about patterns of species diversity. On the other hand, some of the published work that claims to reject the Oscillation Hypothesis may actually provide some of the strongest support for it, and I present new analyses which support its prediction that host-use generalism facilitates host-use evolution. In summary, the Oscillation Hypothesis successfully predicts some phylogenetic patterns but not others. Generalism appears to facilitate host-use evolution, but it does not appear to be inevitably chased by host-use specialization and speciation.

Gene expression plasticity across hosts of an invasive scale insect species.

For plant-eating insects, we still have only a nascent understanding of the genetic basis of host-use promiscuity. Here, to improve that situation, we investigated host-induced gene expression plasticity in the invasive lobate lac scale insect, Paratachardina pseudolobata (Hemiptera: Keriidae). We were particularly interested in the differential expression of detoxification and effector genes, which are thought to be critical for overcoming a plant's chemical defenses. We collected RNA samples from P. pseudolobata on three different host plant species, assembled transcriptomes de novo, and identified transcripts with significant host-induced gene expression changes. Gene expression plasticity was pervasive, but the expression of most detoxification and effector genes was insensitive to the host environment. Nevertheless, some types of detoxification genes were more differentially expressed than expected by chance. Moreover, we found evidence of a trade-off between expression of genes involved in primary and secondary metabolism; hosts that induced lower expression of genes for detoxification induced higher expression of genes for growth. Our findings are largely consonant with those of several recently published studies of other plant-eating insect species. Thus, across plant-eating insect species, there may be a common set of gene expression changes that enable host-use promiscuity.

Micro- and Macroevolutionary Trade-Offs in Plant-Feeding Insects.

A long-standing hypothesis asserts that plant-feeding insects specialize on particular host plants because of negative interactions (trade-offs) between adaptations to alternative hosts, yet empirical evidence for such trade-offs is scarce. Most studies have looked for microevolutionary performance trade-offs within insect species, but host use could also be constrained by macroevolutionary trade-offs caused by epistasis and historical contingency. Here we used a phylogenetic approach to estimate the micro- and macroevolutionary correlations between use of alternative host-plant taxa within two major orders of plant-feeding insects: Lepidoptera (caterpillars) and Hemiptera (true bugs). Across 1,604 caterpillar species, we found both positive and negative pairwise correlations between use of 11 host-plant orders, with overall network patterns suggesting that different host-use constraints act over micro- and macroevolutionary timescales. In contrast, host-use patterns of 955 true bug species revealed uniformly positive correlations between use of the same 11 host plant orders over both timescales. The lack of consistent patterns across timescales and insect orders indicates that host-use trade-offs are historically contingent rather than universal constraints. Moreover, we observed few negative correlations overall despite the wide taxonomic and ecological diversity of the focal host-plant orders, suggesting that positive interactions between host-use adaptations, not trade-offs, dominate the long-term evolution of host use in plant-feeding insects.

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.

ScaleNet: a literature-based model of scale insect biology and systematics.

Scale insects (Hemiptera: Coccoidea) are small herbivorous insects found on all continents except Antarctica. They are extremely invasive, and many species are serious agricultural pests. They are also emerging models for studies of the evolution of genetic systems, endosymbiosis and plant-insect interactions. ScaleNet was launched in 1995 to provide insect identifiers, pest managers, insect systematists, evolutionary biologists and ecologists efficient access to information about scale insect biological diversity. It provides comprehensive information on scale insects taken directly from the primary literature. Currently, it draws from 23,477 articles and describes the systematics and biology of 8194 valid species. For 20 years, ScaleNet ran on the same software platform. That platform is no longer viable. Here, we present a new, open-source implementation of ScaleNet. We have normalized the data model, begun the process of correcting invalid data, upgraded the user interface, and added online administrative tools. These improvements make ScaleNet easier to use and maintain and make the ScaleNet data more accurate and extendable. Database URL: http://scalenet.info.