John O. Stireman

Host specificity of Lepidoptera in tropical and temperate forests

For numerous taxa, species richness is much higher in tropical than in temperate zone habitats. A major challenge in community ecology and evolutionary biogeography is to reveal the mechanisms underlying these differences. For herbivorous insects, one such mechanism leading to an increased number of species in a given locale could be increased ecological specialization, resulting in a greater proportion of insect species occupying narrow niches within a community. We tested this hypothesis by comparing host specialization in larval Lepidoptera (moths and butterflies) at eight different New World forest sites ranging in latitude from 15°u2009S to 55°u2009N. Here we show that larval diets of tropical Lepidoptera are more specialized than those of their temperate forest counterparts: tropical species on average feed on fewer plant species, genera and families than do temperate caterpillars. This result holds true whether calculated per lepidopteran family or for a caterpillar assemblage as a whole. As a result, there is greater turnover in caterpillar species composition (greater β diversity) between tree species in tropical faunas than in temperate faunas. We suggest that greater specialization in tropical faunas is the result of differences in trophic interactions; for example, there are more distinct plant secondary chemical profiles from one tree species to the next in tropical forests than in temperate forests as well as more diverse and chronic pressures from natural enemy communities.

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.

Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions

Ecological specialization is a fundamental and well-studied concept, yet its great reach and complexity limit current understanding in important ways. More than 20 years after the publication of D. J. Futuyma and G. Morenos oft-cited, major review of the topic, we synthesize new developments in the evolution of ecological specialization. Using insect-plant interactions as a model, we focus on important developments in four critical areas: genetic architecture, behavior, interaction complexity, and macroevolution. We find that theory based on simple genetic trade-offs in host use is being replaced by more subtle and complex pictures of genetic architecture, and multitrophic interactions have risen as a necessary framework for understanding specialization. A wealth of phylogenetic data has made possible a more detailed consideration of the macroevolutionary dimension of specialization, revealing (among other things) bidirectionality in transitions between generalist and specialist lineages. Technological advances, including genomic sequencing and analytical techniques at the community level, raise the possibility that the next decade will see research on specialization spanning multiple levels of biological organization in non-model organisms, from genes to populations to networks of interactions in natural communities. Finally, we offer a set of research questions that we find to be particularly pressing and fruitful for future research on ecological specialization.

Phytophagous Insect-Microbe Mutualisms and Adaptive Evolutionary Diversification

Abstract Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.

Cascading host-associated genetic differentiation in parasitoids of phytophagous insects

The extraordinary diversity of phytophagous insects may be attributable to their narrow specialization as parasites of plants, with selective tradeoffs associated with alternate host plants driving genetic divergence of host-associated forms via ecological speciation. Most phytophagous insects in turn are attacked by parasitoid insects, which are similarly specialized and may also undergo host-associated differentiation (HAD). A particularly interesting possibility is that HAD by phytophagous insects might lead to HAD in parasitoids, as parasitoids evolve divergent lineages on the new host plant-specific lineages of their phytophagous hosts. We call this process ‘cascading host-associated differentiation’ (cascading HAD). We tested for cascading HAD in parasitoids of two phytophagous insects, each of which consists of genetically distinct host-associated lineages on the same pair of goldenrods (Solidago). Each parasitoid exhibited significant host-associated genetic divergence, and the distribution and patterns of divergence are consistent with divergence in sympatry. Although evidence for cascading HAD is currently limited, our results suggest that it could play an important role in the diversification of parasitoids attacking phytophagous insects. The existence of cryptic host-associated lineages also suggests that the diversity of parasitoids may be vastly underestimated.

Origins, Distribution, and Local Co-Occurrence Of Polyploid Cytotypes in Solidago Altissima (Asteraceae)

There is growing realization that intraspecific polyploidy in plants has important implications for the evolution of plant diversity and for plant and plant-herbivore community dynamics. Nonetheless, the rate at which polyploid cytotypes arise and their fate in local mixed-cytotype populations are not well understood. Although within- and especially among-population cytotype variation has been documented in many plants, particularly at the largest (continental) spatial scales, local and regional distributions of cytotypes have been well characterized only for a handful of species. Furthermore, few if any studies have addressed both local and regional patterns in the same plant species with sufficient power to detect cytotype variation on both scales. We assessed the co-occurrence and frequency distributions of diploid, tetraploid, and hexaploid cytotypes of Solidago altissima (Asteraceae) at local and regional spatial scales, sampling across a zone of presumed ploidy-form overlap in the midwestern United States. Determining ploidy by flow cytometry, we found many local populations containing two or three cytotypes, with the relative frequencies of cytotypes varying dramatically even among neighboring populations. AFLP marker data suggest that polyploid cytotypes of S. altissima likely have multiple origins from different diploid lineages. Our results are consistent with recent perspectives on polyploidization as an evolutionarily dynamic phenomenon with frequent multiple origins of higher-ploidy cytotypes.

Differential attack on diploid, tetraploid, and hexaploid Solidago altissima L. by five insect gallmakers

Genetic variation among plants can influence host choice and larval performance in insect herbivores. Ploidy (cytotype) variation is a particularly dramatic form of plant genetic variation, and where diploid and polyploid cytotypes of a species occur in sympatry, they may provide herbivores with choices that are distinguished by profound and genome-wide genetic differences. We tested for non-random attack by five gallmaking insect herbivores on diploid, tetraploid, and hexaploid cytotypes of the goldenrod Solidago altissima L., working in seven midwestern US populations where the ploidies co-occur on spatial scales relevant to insect host choice. For four of the five herbivores, attack was non-random with respect to ploidy at one or more sites. Ploidy effects on attack were complex: the ploidy subjected to highest attack varied both across herbivores within sites and (for most herbivores) across sites within herbivores. Ploidy effects on attack will alter rates of encounter between insect herbivores—either increasing or decreasing the likelihood of two herbivores sharing a host plant ramet, compared with the case with no effects of ploidy. Plant ploidy variation appears likely to have a major impact on insect community organization, and perhaps on plant–herbivore coevolution, but that impact is likely to be spatially heterogeneous.

Perennial habitat fragments, parasitoid diversity and parasitism in ephemeral crops

Summary 1. Agricultural intensification has led to the removal of semi-wild, perennial vegetation in agricultural landscapes. However, in short-cycle crops, frequent disturbance from insecticides, harvesting and tillage disrupts the establishment of resident communities of natural enemies of pests. Semi-wild perennial vegetation may provide critical habitat for mobile arthropods supporting ecosystem services and sustainable agriculture. 2. We sampled tachinid parasitoids, an important taxon for biological control of vegetable pests, in 35 organic farm fields situated within a mosaic of agricultural, residential and preserved lands in coastal California. Using a GIS, we characterized land-use and vegetative cover within 500 and 1500 m, including grasslands, chaparral, oak woodlands and coniferous forests. 3. The abundance and species richness of tachinid flies captured in Malaise traps in spring and summer were positively associated with the cover of semi-wild perennial vegetation, especially in mesic habitats. The effective number of tachinid species (e H ) was correlated positively with semi-wild perennial vegetation cover and negatively with annual crop cover in the landscape in September and May. 4. The richness of parasitoids emerging from sentinel lepidopteran pests exposed on potted plants within farm fields was negatively associated with annual cropland cover. Parasitism rates dropped precipitously as percentage annual crop cover exceeded species-specific thresholds. 5. Synthesis and applications. Maintaining semi-wild, perennial habitat fragments as refugia to support parasitoids can increase biodiversity and provide ecosystem services in annual and short-cycle crop fields. Our results indicated that crop pests escaped parasitism by two important tachinid species in landscapes with greater than 38% and 51% cover of annual cropland, respectively. Landscape-level research is critical for integrating science and policy to conserve biodiversity, promote sustainable agroecosystems and evaluate new anti-wildlife vegetation removal campaigns that may harm biological control agents while targeting microbial food

Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals.

Carotenoids are conjugated isoprenoid molecules with many important physiological functions in organisms, including roles in photosynthesis, oxidative stress reduction, vision, diapause, photoperiodism, and immunity. Until recently, it was believed that only plants, microorganisms, and fungi were capable of synthesizing carotenoids and that animals acquired them from their diet, but recent studies have demonstrated that two arthropods (pea aphid and spider mite) possess a pair of genes homologous to those required for the first step of carotenoid biosynthesis. Absent in all other known animal genomes, these genes appear to have been acquired by aphids and spider mites in one or several lateral gene transfer events from a fungal donor. We report the third case of fungal carotenoid biosynthesis gene homologs in an arthropod: flies from the family Cecidomyiidae, commonly known as gall midges. Using phylogenetic analyses we show that it is unlikely that lycopene cyclase/phytoene synthase and phytoene desaturase homologs were transferred singly to an ancient arthropod ancestor; instead we propose that genes were transferred independently from related fungal donors after divergence of the major arthropod lineages. We also examine variation in intron placement and copy number of the carotenoid genes that may underlie function in the midges. This trans-kingdom transfer of carotenoid genes may represent a key innovation, underlying the evolution of phytophagy and plant-galling in gall midges and facilitating their extensive diversification across plant lineages.

Spatial and temporal variation in the parasitoid assemblage of an exophytic polyphagous caterpillar

Abstract 1. Over 3400 larvae of the polyphagous ground dwelling arctiid Grammia geneura were sampled and reared over seven generations in order to characterise its parasitoid assemblage and examine how and why this assemblage varies over time and space at a variety of scales.