Intra- and interspecific diversity in a tropical plant clade alter herbivory and ecosystem resilience.

Declines in biodiversity generated by anthropogenic stressors at both species and population levels can alter emergent processes instrumental to ecosystem function and resilience. As such, understanding the role of biodiversity in ecosystem function and its response to climate perturbation is increasingly important, especially in tropical systems where responses to changes in biodiversity are less predictable and more challenging to assess experimentally. Using large-scale transplant experiments conducted at five neotropical sites, we documented the impacts of changes in intraspecific and interspecific plant richness in the genus Piper on insect herbivory, insect richness, and ecosystem resilience to perturbations in water availability. We found that reductions of both intraspecific and interspecific Piper diversity had measurable and site-specific effects on herbivory, herbivorous insect richness, and plant mortality. The responses of these ecosystem-relevant processes to reduced intraspecific Piper richness were often similar in magnitude to the effects of reduced interspecific richness. Increased water availability reduced herbivory by 4.2% overall, and the response of herbivorous insect richness and herbivory to water availability were altered by both intra- and interspecific richness in a site-dependent manner. Our results underscore the role of intraspecific and interspecific richness as foundations of ecosystem function and the importance of community and location-specific contingencies in controlling function in complex tropical systems.

Two new species of the hyperdiverse geometrid moth genus Eois (Lepidoptera, Geometridae, Larentiinae) from Ecuador, with descriptions of early stages.

The hyperdiverse geometrid genus Eois Hübner, estimated to encompass more than 1,000 species, is among the most species-rich genera in all of Lepidoptera. While the genus has attracted considerable attention from ecologists and evolutionary biologists in recent decades, limited progress has been made on its alpha taxonomy. This contribution focuses on the Olivacea clade, whose monophyly has been recognized previously through molecular analyses. We attempt to define the clade from a morphological perspective and recognize the following species based on morphology and genomic data: E.olivacea (Felder & Rogenhofer); E.pseudolivacea Doan, sp. nov.; E.auruda (Dognin), stat. rev.; E.beebei (Fletcher, 1952), stat. rev.; E.boliviensis (Dognin), stat. rev.; and E.parumsimii Doan, sp. nov. Descriptions and illustrations of the immature stages of E.pseudolivacea reared from Piper (Piperaceae) in Ecuador are provided.

Host plant-mediation of viral transmission and its consequences for a native butterfly.

Pathogens play a key role in insect population dynamics, contributing to short-term fluctuations in abundance as well as long-term demographic trends. Two key factors that influence the effects of entomopathogens on herbivorous insect populations are modes of pathogen transmission and larval host plants. In this study, we examined tritrophic interactions between a sequestering specialist lepidopteran, Euphydryas phaeton, and a viral pathogen, Junonia coenia densovirus, on its native host plant, Chelone glabra, and a novel host plant, Plantago lanceolata, to explore whether host plant mediates viral transmission, survival, and viral loads. A two-factor factorial experiment was conducted in the laboratory with natal larval clusters randomly assigned to either the native or novel host plant and crossed with either uninoculated controls or viral inoculation (20% of individuals in the cluster inoculated). Diapausing clusters were overwintered in the laboratory and checked weekly for mortality. At the end of diapause, all surviving individuals were reared to adulthood to estimate survivorship. All individuals were screened to quantify viral loads, and estimate horizontal transmission postmortem. To test for vertical transmission, adults were mated, and the progeny were screened for viral presence. Within virus-treated groups, we found evidence for both horizontal and vertical transmission. Larval clusters reared on the native host plant had slightly higher horizontal transmission. Survival probability was lower in clusters feeding on the native host plant, with inoculated groups reared on the native host plant experiencing complete mortality. Viral loads did not differ by the host plant, although viral loads decreased with increased sequestration of secondary compounds on both host plants. Our results indicate that the use of a novel host plant may confer fitness benefits in terms of survival and reduced viral transmission when larvae feeding on it are infected with this pathogen, supporting hypotheses of potential evolutionary advantages of a host range expansion in the context of tritrophic interactions.

Sparse modeling for climate variable selection across trophic levels.

Understanding how populations respond to climate is fundamentally important to many questions in ecology, evolution, and conservation biology. Climate is complex and multifaceted, with aspects affecting populations in different and sometimes unexpected ways. Thus, when measuring the changing climate it is important to consider the complexity of the phenomenon and the number of ways it can be characterized through different metrics. We used a Bayesian sparse modeling approach to select among 80 metrics of climate and applied the approach to 19 datasets of bird, insect, and plant population responses to abiotic conditions as case studies of how the method can be applied for climate variable selection in a time series context. For phenological datasets, mean spring temperature was frequently selected as an important climate driver, while selected predictors were more diverse for population metrics such as abundance or reproductive success. The climate variable selection approach presented here can help to identify potential climate metrics when there is limited physiological or mechanistic information to make an a priori variable selection, and is broadly applicable across studies on population responses to climate.

Thirty-six years of butterfly monitoring, snow cover, and plant productivity reveal negative impacts of warmer winters and increased productivity on montane species.

Climate change is contributing to declines of insects through rising temperatures, altered precipitation patterns, and an increasing frequency of extreme events. The impacts of both gradual and sudden shifts in weather patterns are realized directly on insect physiology and indirectly through impacts on other trophic levels. Here, we investigated direct effects of seasonal weather on butterfly occurrences and indirect effects mediated by plant productivity using a temporally intensive butterfly monitoring dataset, in combination with high-resolution climate data and a remotely sensed indicator of plant primary productivity. Specifically, we used Bayesian hierarchical path analysis to quantify relationships between weather and weather-driven plant productivity on the occurrence of 94 butterfly species from three localities distributed across an elevational gradient. We found that snow pack exerted a strong direct positive effect on butterfly occurrence and that low snow pack was the primary driver of reductions during drought. Additionally, we found that plant primary productivity had a consistently negative effect on butterfly occurrence. These results highlight mechanisms of weather-driven declines in insect populations and the nuances of climate change effects involving snow melt, which have implications for ecological theories linking topographic complexity to ecological resilience in montane systems.

Does a history of population co-occurrence predict plant performance, community productivity, or invasion resistance?

A history of species co-occurrence in plant communities is hypothesized to lead to greater niche differentiation, more efficient resource partitioning, and more productive, resistant communities as a result of evolution in response to biotic interactions. A similar question can be asked of co-occurring populations: do individual species or community responses differ when communities are founded with plants sharing a history of population co-occurrence (sympatric) or originating from different locations (allopatric)? Using shrub, grass, and forb species from six locations in the western Great Basin, North America, we compared establishment, productivity, reproduction, phenology, and resistance to invaders for experimental communities with either sympatric or allopatric population associations. Each community type was planted with six taxa in outdoor mesocosms, measured over three growing seasons, and invaded with the annual grass Bromus tectorum in the final season. For most populations, the allopatric or sympatric status of neighbors was not important. However, in some cases, it was beneficial for some species from some locations to be planted with allopatric neighbors, while others benefited from sympatric neighbors, and some of these responses had large effects. For instance, the Elymus population that benefited the most from allopatry grew 50% larger with allopatric neighbors than in single origin mesocosms. This response affected invasion resistance, as B. tectorum biomass was strongly affected by productivity and phenology of Elymus spp., as well as Poa secunda. Our results demonstrate that, while community composition can affect plant performance in semi-arid plant communities, assembling communities from sympatric populations is not sufficient to ensure high productivity and invasion resistance. Instead, we observed an idiosyncratic interaction between sampling effects and evolutionary history, with the potential for seed source of individual populations to have community-level effects.

Additive and interactive effects of anthropogenic stressors on an insect herbivore.

The pressures of global change acting on wild plants and animals include exposure to environmental toxins, the introduction of non-native species, and climate change. Relatively few studies have been reported in which these three main classes of stressors have been examined simultaneously, allowing for the possibility of synergistic effects in an experimental context. In this study, we exposed caterpillars of the Melissa blue butterfly (Lycaeides melissa) to three concentrations of chlorantraniliprole, under three experimental climates, on a diet of a native or a non-native host plant throughout larval development in a fully factorial experiment. We find that high pesticide exposure and a non-native diet exhibit strong negative effects on caterpillars, resulting in 62% and 42% reduction in survival, respectively, while interactive effects tend to be weaker, ranging from 15% to 22% reduction in survival. Interactive effects have been shown to be strong in other contexts, but do not appear to be universal; however, our study shows that the cumulative effects of stressors acting in isolation (additively) are sufficiently strong to severely reduce survival and by extension population persistence in the wild.

Agricultural margins could enhance landscape connectivity for pollinating insects across the Central Valley of California, U.S.A.

One of the defining features of the Anthropocene is eroding ecosystem services, decreases in biodiversity, and overall reductions in the abundance of once-common organisms, including many insects that play innumerable roles in natural communities and agricultural systems that support human society. It is now clear that the preservation of insects cannot rely solely on the legal protection of natural areas far removed from the densest areas of human habitation. Instead, a critical challenge moving forward is to intelligently manage areas that include intensively farmed landscapes, such as the Central Valley of California. Here we attempt to meet this challenge with a tool for modeling landscape connectivity for insects (with pollinators in particular in mind) that builds on available information including lethality of pesticides and expert opinion on insect movement. Despite the massive fragmentation of the Central Valley, we find that connectivity is possible, especially utilizing the restoration or improvement of agricultural margins, which (in their summed area) exceed natural areas. Our modeling approach is flexible and can be used to address a wide range of questions regarding both changes in land cover as well as changes in pesticide application rates. Finally, we highlight key steps that could be taken moving forward and the great many knowledge gaps that could be addressed in the field to improve future iterations of our modeling approach.

Extreme drought disrupts plant phenology: Insights from 35 years of cloud forest data in Venezuela.

The potential effects of climate change on plant reproductive phenology include asynchronies with pollinators and reductions in plant fitness, leading to extinction and loss of ecosystem function. In particular, plant phenology is sensitive to extreme weather events, which are occurring with increasing severity and frequency in recent decades and are linked to anthropogenic climate change and shifts in atmospheric circulation. For 15 plant species in a Venezuelan cloud forest, we documented dramatic changes in monthly flower and fruit community composition over a 35-year time series, from 1983 to 2017, and these changes were linked directly to higher temperatures, lower precipitation, and decreased soil water availability. The patterns documented here do not mirror trends in temperate zones but corroborate results from the Asian tropics. More intense droughts are predicted to occur in the region, which will cause dramatic changes in flower and fruit availability.

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.

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 continental-scale survey of Wolbachia infections in blue butterflies reveals evidence of interspecific transfer and invasion dynamics.

Infections by maternally inherited bacterial endosymbionts, especially Wolbachia, are common in insects and other invertebrates but infection dynamics across species ranges are largely under studied. Specifically, we lack a broad understanding of the origin of Wolbachia infections in novel hosts, and the historical and geographical dynamics of infections that are critical for identifying the factors governing their spread. We used Genotype-by-Sequencing data from previous population genomics studies for range-wide surveys of Wolbachia presence and genetic diversity in North American butterflies of the genus Lycaeides. As few as one sequence read identified by assembly to a Wolbachia reference genome provided high accuracy in detecting infections in host butterflies as determined by confirmatory PCR tests, and maximum accuracy was achieved with a threshold of only 5 sequence reads per host individual. Using this threshold, we detected Wolbachia in all but 2 of the 107 sampling localities spanning the continent, with infection frequencies within populations ranging from 0% to 100% of individuals, but with most localities having high infection frequencies (mean = 91% infection rate). Three major lineages of Wolbachia were identified as separate strains that appear to represent 3 separate invasions of Lycaeides butterflies by Wolbachia. Overall, we found extensive evidence for acquisition of Wolbachia through interspecific transfer between host lineages. Strain wLycC was confined to a single butterfly taxon, hybrid lineages derived from it, and closely adjacent populations in other taxa. While the other 2 strains were detected throughout the rest of the continent, strain wLycB almost always co-occurred with wLycA. Our demographic modeling suggests wLycB is a recent invasion. Within strain wLycA, the 2 most frequent haplotypes are confined almost exclusively to separate butterfly taxa with haplotype A1 observed largely in Lycaeides melissa and haplotype A2 observed most often in Lycaeides idas localities, consistent with either cladogenic mode of infection acquisition from a common ancestor or by hybridization and accompanying mutation. More than 1 major Wolbachia strain was observed in 15 localities. These results demonstrate the utility of using resequencing data from hosts to quantify Wolbachia genetic variation and infection frequency and provide evidence of multiple colonizations of novel hosts through hybridization between butterfly lineages and complex dynamics between Wolbachia strains.

Jack-of-all-trades paradigm meets long-term data: Generalist herbivores are more widespread and locally less abundant.

Insect herbivores are relatively specialized. Why this is so is not clear. We examine assumptions about associations between local abundance and dietary specialization using an 18-year data set of caterpillar-plant interactions in Ecuador. Our data consist of caterpillar-plant associations and include standardized plot-based samples and general collections of caterpillars, allowing for diet breadth and abundance estimates across spatial scales for 1917 morphospecies. We find that more specialized caterpillars are locally more abundant than generalists, consistent with a key component of the 'jack of all trades, master of none' hypothesis. As the diet breadth of species increased, generalists were not as abundant in any one location, but they had broader occupancy across the landscape, which is a pattern that could reflect high plant beta diversity and is consistent with an alternative neutral hypothesis. Our finding that more specialized species can be both rare and common highlights the ecological complexity of specialization.

Phytochemistry reflects different evolutionary history in traditional classes versus specialized structural motifs.

Foundational hypotheses addressing plant-insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. However, numerous studies have documented variation in the degree of phytochemical trait lability, raising the possibility that phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance (1H NMR) data, chemical classification, and double digest restriction-site associated DNA sequencing (ddRADseq) to resolve evolutionary relationships and characterize the evolution of secondary chemistry in the Neotropical plant clade Radula (Piper; Piperaceae). Sequencing data substantially improved phylogenetic resolution relative to past studies, and spectroscopic characterization revealed the presence of 35 metabolite classes. Metabolite classes displayed phylogenetic signal, whereas the crude 1H NMR spectra featured little evidence of phylogenetic signal in multivariate tests of chemical resonances. Evolutionary correlations were detected in two pairs of compound classes (flavonoids with chalcones; p-alkenyl phenols with kavalactones), where the gain or loss of a class was dependent on the other's state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.

A suite of rare microbes interacts with a dominant, heritable, fungal endophyte to influence plant trait expression.

Endophytes are microbes that live, for at least a portion of their life history, within plant tissues. Endophyte assemblages are often composed of a few abundant taxa and many infrequently observed, low-biomass taxa that are, in a word, rare. The ways in which most endophytes affect host phenotype are unknown; however, certain dominant endophytes can influence plants in ecologically meaningful ways-including by affecting growth and immune system functioning. In contrast, the effects of rare endophytes on their hosts have been unexplored, including how rare endophytes might interact with abundant endophytes to shape plant phenotype. Here, we manipulate both the suite of rare foliar endophytes (including both fungi and bacteria) and Alternaria fulva-a vertically transmitted and usually abundant fungus-within the fabaceous forb Astragalus lentiginosus. We report that rare, low-biomass endophytes affected host size and foliar %N, but only when the heritable fungal endophyte (A. fulva) was not present. A. fulva also reduced plant size and %N, but these deleterious effects on the host could be offset by a negative association we observed between this heritable fungus and a foliar pathogen. These results demonstrate how interactions among endophytic taxa determine the net effects on host plants and suggest that the myriad rare endophytes within plant leaves may be more than a collection of uninfluential, commensal organisms, but instead have meaningful ecological roles.

Insects and recent climate change.

Insects have diversified through more than 450 million y of Earth's changeable climate, yet rapidly shifting patterns of temperature and precipitation now pose novel challenges as they combine with decades of other anthropogenic stressors including the conversion and degradation of land. Here, we consider how insects are responding to recent climate change while summarizing the literature on long-term monitoring of insect populations in the context of climatic fluctuations. Results to date suggest that climate change impacts on insects have the potential to be considerable, even when compared with changes in land use. The importance of climate is illustrated with a case study from the butterflies of Northern California, where we find that population declines have been severe in high-elevation areas removed from the most immediate effects of habitat loss. These results shed light on the complexity of montane-adapted insects responding to changing abiotic conditions. We also consider methodological issues that would improve syntheses of results across long-term insect datasets and highlight directions for future empirical work.

Thistledown velvet ants in the Desert Mimicry Ring and the evolution of white coloration: Müllerian mimicry, camouflage and thermal ecology.

Adaptive coloration among animals is one of the most recognizable outcomes of natural selection. Here, we investigate evolutionary drivers of white coloration in velvet ants (Hymenoptera: Mutillidae), which has previously been considered camouflage with the fruit of creosote bush (Larrea tridentata). Our analyses indicate instead that velvet ants evolved white coloration millions of years before creosote bush was widespread in North America's hot deserts. Furthermore, velvet ants and the creosote fruit exhibit different spectral reflectance patterns, which appear distinct to potential insectivorous predators. While the white coloration in velvet ants likely did not evolve as camouflage, we find that white-coloured species remain cooler than their red/orange relatives, and therefore we infer the white coloration likely evolved in response to Neogene desertification. This study shows the importance of cross-disciplinary investigation and of testing multiple hypotheses when investigating evolutionary drivers of adaptive coloration.

Caterpillars on a phytochemical landscape: The case of alfalfa and the Melissa blue butterfly.

Modern metabolomic approaches that generate more comprehensive phytochemical profiles than were previously available are providing new opportunities for understanding plant-animal interactions. Specifically, we can characterize the phytochemical landscape by asking how a larger number of individual compounds affect herbivores and how compounds covary among plants. Here we use the recent colonization of alfalfa (Medicago sativa) by the Melissa blue butterfly (Lycaeides melissa) to investigate the effects of indivdiual compounds and suites of covarying phytochemicals on caterpillar performance. We find that survival, development time, and adult weight are all associated with variation in nutrition and toxicity, including biomolecules associated with plant cell function as well as putative anti-herbivore action. The plant-insect interface is complex, with clusters of covarying compounds in many cases encompassing divergent effects on different aspects of caterpillar performance. Individual compounds with the strongest associations are largely specialized metabolites, including alkaloids, phenolic glycosides, and saponins. The saponins are represented in our data by more than 25 individual compounds with beneficial and detrimental effects on L. melissa caterpillars, which highlights the value of metabolomic data as opposed to approaches that rely on total concentrations within broad defensive classes.