Convergence and Divergence among Herbivorous Insects Specialized on Toxic Plants: Revealing Syndromes among the Cardenolide Feeders across the Insect Tree of Life.

AbstractRepeatable macroevolutionary patterns provide hope for rules in biology, especially when we can decipher the underlying mechanisms. Here we synthesize natural history, genetic adaptations, and toxin sequestration in herbivorous insects that specialize on plants with cardiac glycoside defenses. Work on the monarch butterfly provided a model for evolution of the "sequestering specialist syndrome," where specific amino acid substitutions in the insect's Na+/K+-ATPase are associated with (1) high toxin resistance (target site insensitivity [TSI]), (2) sequestration of toxins, and (3) aposematic coloration. We evaluate convergence for these traits within and between Lepidoptera, Coleoptera, Diptera, Hemiptera, Hymenoptera, and Orthoptera, encompassing hundreds of toxin-adapted species. Using new and existing data on ∼28 origins of specialization, we show that the monarch model evolved independently in five taxonomic orders (but not Diptera). An additional syndrome occurs in five orders (all but Hymenoptera): aposematic sequesterers with modest to medium TSI. Indeed, all sequestering species were aposematic, and all but one had at least modest TSI. Additionally, several species were aposematic nonsequesterers (potential Batesian mimics), and this combination evolved in species with a range of TSI levels. Finally, we identified some biases among these strategies within taxonomic orders. Biodiversity in this microcosm of life evolved repeatedly with a high degree of similarity across six taxonomic orders, yet we identified alternative trait combinations as well as lineage-specific outcomes.

Lineage-specific patterns of chromosome evolution are the rule not the exception in Polyneoptera insects.

The structure of a genome can be described at its simplest by the number of chromosomes and the sex chromosome system it contains. Despite over a century of study, the evolution of genome structure on this scale remains recalcitrant to broad generalizations that can be applied across clades. To address this issue, we have assembled a dataset of 823 karyotypes from the insect group Polyneoptera. This group contains orders with a range of variations in chromosome number, and offer the opportunity to explore the possible causes of these differences. We have analysed these data using both phylogenetic and taxonomic approaches. Our analysis allows us to assess the importance of rates of evolution, phylogenetic history, sex chromosome systems, parthenogenesis and genome size on variation in chromosome number within clades. We find that fusions play a key role in the origin of new sex chromosomes, and that orders exhibit striking differences in rates of fusions, fissions and polyploidy. Our results suggest that the difficulty in finding consistent rules that govern evolution at this scale may be due to the presence of many interacting forces that can lead to variation among groups.

Endosymbionts facilitate rapid evolution in a polyphagous herbivore.

Maternally transmitted bacterial symbionts can be important mediators of the interactions between insect herbivores and their foodplants. These symbionts are often facultative (present in some host individuals but not others) and can have large effects on their host's phenotype, thus giving rise to heritable variation upon which selection can act. In the cowpea aphid (Aphis craccivora), it has been established that the facultative endosymbiont Arsenophonus improves aphid performance on black locust trees (Robinia pseudoacacia) but not on fava (Vicia faba). Here, we tested whether this fitness differential translated into contemporaneous evolution of aphid populations associated with the different plants. In a laboratory study lasting 16 weeks, we found that the frequency of Arsenophonus-infected individuals significantly increased over time for aphid populations on black locust but declined for aphid populations on fava. By the end of the experiment, Arsenophonus infection was >3× more common on black locust than fava, which is comparable to previously described infection frequencies in natural field populations. Our results clearly demonstrate that aphid populations with mixed facultative symbiont infection status can rapidly evolve in response to the selective environments imposed by different host plants. This selection differential may be a sufficient explanation for the global association between Arsenophonus-infected cowpea aphids and black locust trees, without invoking additional assortative mechanisms. Because the aphid and plant originate from different parts of the world, we further hypothesize that Arsenophonus infection may have acted as a preadaptation that has promoted functional specialization of infected aphids on a novel host plant.

Heritable variation in prey defence provides refuge for subdominant predators.

Generalist predators with broadly overlapping niches commonly coexist on seemingly identical sets of prey. Here, we provide empirical demonstration that predators can differentially exploit fine-grained niches generated by variable, heritable and selective defences within a single prey species. Some, but not all, clones of the aphid Aphis craccivora are toxic towards the dominant invasive predatory ladybeetle, Harmonia axyridis However, other less competitive ladybeetle species are not affected by the aphid's toxic trait. In laboratory and open field experiments, we show: (i) that subdominant ladybeetle species were able to exploit the toxic aphids, benefitting from the suppression of the dominant predator; and (ii) that this narrow-spectrum toxicity can function as an anti-predator defence for the aphid, but depends on enemy community context. Our results demonstrate that niche differentiation among generalist predators may hinge upon previously underappreciated heritable variation in prey defence, which, in turn, may promote diversity and stability of enemy communities invaded by a dominant predator.

Field Documentation of Unusual Post-Mortem Arthropod Activity on Human Remains.

During a forensic investigation, the presence of physical marks on human remains can influence the interpretation of events related to the death of an individual. Some tissue injury on human remains can be misinterpreted as ante- or peri-mortem wounds by an investigator when in reality the markings resulted from post-mortem arthropod activity. Unusual entomological data were collected during a study examining the decomposition of a set of human remains in San Marcos, Texas. An adult female Pediodectes haldemani (Girard) (Orthoptera: Tettigoniidae) and an Armadillidium cf. vulgare (Isopoda: Armadilidiidae) were documented feeding on the remains. Both arthropods produced physical marks or artifacts on the remains that could be misinterpreted as attack, abuse, neglect, or torture. Additionally, red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae), were observed constructing structures in the mark produced by the P. haldemani feeding. These observations provide insight into the potential of post-mortem arthropod damage to human remains, which previously had not been described for these taxa, and therefore, physical artifacts on any remains found in similar circumstances may result from arthropod activity and not ante- or peri-mortem wounds.

Quantifying Plant Soluble Protein and Digestible Carbohydrate Content, Using Corn (Zea mays) As an Exemplar.

Elemental data are commonly used to infer plant quality as a resource to herbivores. However, the ubiquity of carbon in biomolecules, the presence of nitrogen-containing plant defensive compounds, and variation in species-specific correlations between nitrogen and plant protein content all limit the accuracy of these inferences. Additionally, research focused on plant and/or herbivore physiology require a level of accuracy that is not achieved using generalized correlations. The methods presented here offer researchers a clear and rapid protocol for directly measuring plant soluble proteins and digestible carbohydrates, the two plant macronutrients most closely tied to animal physiological performance. The protocols combine well characterized colorimetric assays with optimized plant-specific digestion steps to provide precise and reproducible results. Our analyses of different sweet corn tissues show that these assays have the sensitivity to detect variation in plant soluble protein and digestible carbohydrate content across multiple spatial scales. These include between-plant differences across growing regions and plant species or varieties, as well as within-plant differences in tissue type and even positional differences within the same tissue. Combining soluble protein and digestible carbohydrate content with elemental data also has the potential to provide new opportunities in plant biology to connect plant mineral nutrition with plant physiological processes. These analyses also help generate the soluble protein and digestible carbohydrate data needed to study nutritional ecology, plant-herbivore interactions and food-web dynamics, which will in turn enhance physiology and ecological research.

Using plant nutrient landscapes to assess Anthropocene effects on insect herbivores.

Global climate change will dramatically affect insect herbivores through changes in plant quality. Linking how multiple climate factors affect plant macronutrient content may be the most accurate way to understand the response of insect herbivores. Studies should embrace the complexity of interacting climate factors in natural systems and characterize shifts in multidimensional plant nutrient landscapes. This nutrient landscape simplifies interpretation of climate effects, although selection of appropriate currencies, scale, and interactions with allelochemicals present challenges. By assessing climate change through the filter of nutrient landscapes we could gain an understanding of how complex interacting climate change drivers affect the 'buffet' available to different insect herbivores.