Joshua P. Jahner

The global distribution of diet breadth in insect herbivores

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration. Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

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.

The evolution of novel host use is unlikely to be constrained by trade‐offs or a lack of genetic variation

The genetic and ecological factors that shape the evolution of animal diets remain poorly understood. For herbivorous insects, the expectation has been that trade‐offs exist, such that adaptation to one host plant reduces performance on other potential hosts. We investigated the genetic architecture of alternative host use by rearing individual Lycaeides melissa butterflies from two wild populations in a crossed design on two hosts (one native and one introduced) and analysing the genetic basis of differences in performance using genomic approaches. Survival during the experiment was highest when butterfly larvae were reared on their natal host plant, consistent with local adaptation. However, cross‐host correlations in performance among families (within populations) were not different from zero. We found that L. melissa populations possess genetic variation for larval performance and variation in performance had a polygenic basis. We documented very few genetic variants with trade‐offs that would inherently constrain diet breadth by preventing the optimization of performance across hosts. Instead, most genetic variants that affected performance on one host had little to no effect on the other host. In total, these results suggest that genetic trade‐offs are not the primary cause of dietary specialization in L. melissa butterflies.

The race is not to the swift: Long-term data reveal pervasive declines in California's low-elevation butterfly fauna

Understanding the ecology of extinction is one of the primary challenges facing ecologists in the 21st century. Much of our current understanding of extinction, particularly for invertebrates, comes from studies with large geographic coverage but less temporal resolution, such as comparisons between historical collection records and contemporary surveys for geographic regions or political entities. We present a complementary approach involving a data set that is geographically restricted but temporally intensive: we focus on three sites in the Central Valley of California, and utilize 35 years of biweekly (every two weeks) surveys at our most long-sampled site. Previous analyses of these data revealed declines in richness over recent decades. Here, we take a more detailed approach to investigate the mode of decline for this fauna. We ask if all species are in decline, or only a subset. We also investigate traits commonly found to be predictors of extinction risk in other studies, such as body size, diet breadth, habitat association, and geographic range. We find that population declines are ubiquitous: the majority of species at our three focal sites (but not at a nearby site at higher elevation) are characterized by reductions in the fraction of days that they are observed per year. These declines are not readily predicted by ecological traits, with the possible exception of ruderal/non-ruderal status. Ruderal species, in slightly less precipitous decline than non-ruderal taxa, are more dispersive and more likely to be associated with disturbed habitats and exotic hosts. We conclude that population declines and extirpation, particularly in regions severely and recently impacted by anthropogenic alteration, might not be as predictable as has been suggested by other studies on the ecology of extinction.

Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars

Summary Chemically mediated plant–herbivore interactions contribute to the diversity of terrestrial communities and the diversification of plants and insects. While our understanding of the processes affecting community structure and evolutionary diversification has grown, few studies have investigated how trait variation shapes genetic and species diversity simultaneously in a tropical ecosystem. We investigated secondary metabolite variation among subpopulations of a single plant species, Piper kelleyi (Piperaceae), using high‐performance liquid chromatography (HPLC), to understand associations between plant phytochemistry and host‐specialized caterpillars in the genus Eois (Geometridae: Larentiinae) and associated parasitoid wasps and flies. In addition, we used a genotyping‐by‐sequencing approach to examine the genetic structure of one abundant caterpillar species, Eois encina, in relation to host phytochemical variation. We found substantive concentration differences among three major secondary metabolites, and these differences in chemistry predicted caterpillar and parasitoid community structure among host plant populations. Furthermore, E. encina populations located at high elevations were genetically different from other populations. They fed on plants containing high concentrations of prenylated benzoic acid. Thus, phytochemistry potentially shapes caterpillar and wasp community composition and geographic variation in species interactions, both of which can contribute to diversification of plants and insects.

Specificity, rank preference, and the colonization of a non-native host plant by the Melissa blue butterfly

Animals often express behavioral preferences for different types of food or other resources, and these preferences can evolve or shift following association with novel food types. Shifts in preference can involve at least two phenomena: a change in rank preference or a change in specificity. The former corresponds to a change in the order in which hosts are preferred, while a shift in specificity can be an increase in the tendency to utilize multiple hosts. These possibilities have been examined in relatively few systems that include extensive population-level replication. The Melissa blue butterfly, Lycaeides melissa, has colonized exotic alfalfa, Medicago sativa, throughout western North America. We assayed the host preferences of 229 females from ten populations associated with novel and native hosts. In four out of five native-associated populations, a native host was preferred over the exotic host, while preference for a native host characterized only two out of five of the alfalfa-associated populations. Across all individuals from alfalfa-associated populations, there appears to have been a decrease in specificity: females from these populations lay fewer eggs on the native host and more eggs on the exotic relative to females from native-host populations. However, females from alfalfa-associated populations did not lay more eggs on a third plant species, which suggests that preferences for specific hosts in this system can potentially be gained and lost independently. Geographic variation in oviposition preference in L. melissa highlights the value of surveying a large number of populations when studying the evolution of a complex behavioral trait.

North American velvet ants form one of the world’s largest known Müllerian mimicry complexes

Color mimicry is often celebrated as one of the most straightforward examples of evolution by natural selection, as striking morphological similarity between species evolves in response to a shared predation pressure. Recently, a large North American mimetic complex was described that included 65 species of Dasymutilla velvet ants (Hymenoptera: Mutillidae). Beyond those 65 species, little is known about how many species participate in this unique Müllerian complex, though several other arthropods are thought to be involved as Müllerian mimics (spider wasps) and Batesian mimics (beetles, antlions, and spiders; see references in). Müllerian mimicry is similarity in appearance or phenotype among harmful species, while Batesian mimicry is similarity in which not all species are harmful. Here, we investigate the extent of the velvet ant mimicry complex beyond Dasymutilla by examining distributional and color pattern similarities in all of the 21 North American diurnal velvet ant genera, including 302 of the 361 named species (nearly 84%), as well as 16 polymorphic color forms and an additional 33 undescribed species. Of the 351 species and color forms that were analyzed (including undescribed species), 336 exhibit some morphological similarities and we hypothesize that they form eight distinct mimicry rings (Figure 1A; Supplemental Information). Two of these eight mimicry rings, red-headed Timulla and black-headed Timulla, were not documented in earlier assessments of mimicry in velvet ants, and are newly described here. These findings identify one of the largest known Müllerian mimicry systems worldwide and provide a novel system to test hypotheses about aposematism and mimicry, especially those regarding the evolution of imperfect mimicry.

Drivers of hybridization in a 66-generation record of Colias butterflies.

Hybridization significantly affects the ecology and evolution of numerous plant and animal lineages. Most studies have focused on endogenous drivers of hybridization and neglected variation in exogenous factors, such as seasonal weather patterns. In this study, we take advantage of a unique dataset consisting of records of hybridization between the butterflies Colias eurytheme and C. eriphyle (Pieridae) for 66 generations (22 years) to investigate the importance of seasonal weather on the production and survival of hybrid offspring. Important seasonal weather variables for each parental species and hybrid offspring were determined using model averaging, and these weather variables, along with butterfly abundances, were analyzed using path analysis. The most important drivers of hybridization were the abundance of C. eriphyle, summer minimum temperature, and spring maximum temperature. In contrast, the abundance of C. eurytheme and weather variables prior to the current flight season were relatively unimportant for variation in hybrid abundance. Parental abundances were mostly driven by weather variables prior to the flight season possibly because these variables affect host plant quality. Our results suggest that exogenous, climatic factors can influence hybridization in natural systems, and that these factors can act both directly on hybrid abundance and indirectly through the population dynamics of parental species.

Ecological and Evolutionary Processes Drive the Origin and Maintenance of Imperfect Mimicry

Although the forces behind the evolution of imperfect mimicry remain poorly studied, recent hypotheses suggest that relaxed selection on small-bodied individuals leads to imperfect mimicry. While evolutionary history undoubtedly affects the development of imperfect mimicry, ecological community context has largely been ignored and may be an important driver of imperfect mimicry. Here we investigate how evolutionary and ecological contexts might influence mimetic fidelity in Müllerian and Batesian mimicry systems. In Batesian hoverfly systems we find that body size is not a strong predictor of mimetic fidelity. However, in Müllerian velvet ants we find a weak positive relationship between body size and mimetic fidelity when evolutionary context is controlled for and a much stronger relationship between community diversity and mimetic fidelity. These results suggest that reduced selection on small-bodied individuals may not be a major driver of the evolution of imperfect mimicry and that other factors, such as ecological community context, should be considered when studying the evolution of imperfect mimicry.

Fine-scale genetic structure among greater sage-grouse leks in central Nevada

BackgroundMating systems that reduce dispersal and lead to non-random mating might increase the potential for genetic structure to arise at fine geographic scales. Greater sage-grouse (Centrocercus urophasianus) have a lek-based mating system and exhibit high site fidelity and skewed mating ratios. We quantified population structure by analyzing variation at 27,866 single-nucleotide polymorphisms in 140 males from ten leks (within five lek complexes) occurring in a small geographic region in central Nevada.ResultsLek complexes, and to a lesser extent individual leks, formed statistically identifiable clusters in ordination analyses, providing evidence for fine-scale geographic genetic differentiation. Lek geography predicted genetic differentiation even at a small geographic scale, which could be sharpened by strong site fidelity. Relatedness was also higher among individuals within lek complexes (and leks), suggesting that reproductive skew, where few males participate in most of the successful matings, could also potentially contribute to genetic differentiation. Models incorporating a habitat resistance surface as a proxy for potentially reduced movement due to landscape features indicated that both geographic distance and habitat suitability (i.e. preferred habitat) predicted genetic structure, with no significant effect of man-made barriers to movement (i.e. power lines and roads). Finally, we illustrate how data sets containing fewer loci (<4000) had less statistical precision and failed to detect the full degree of genetic structure.ConclusionOur results suggest that habitat features and lek site geography of sage-grouse shape fine scale genetic structure, and highlight how larger data sets can have increased precision and accuracy for quantifying ecologically relevant genetic structure over small geographic scales.