Publications

DOI 10.1007/s00114-016-1409-5 

Plant-herbivore interactions have evolved in the presence of plant-colonizing microbes. These microbes can have important third-party effects on herbivore ecology, as exemplified by drosophilid flies that evolved from ancestors feeding on plant-associated microbes. Leaf-mining flies in the genus Scaptomyza, which is nested within the paraphyletic genus Drosophila, show strong associations with bacteria in the genus Pseudomonas, including Pseudomonas syringae. Adult females are capable of vectoring these bacteria between plants and larvae show a preference for feeding on P. syringae-infected leaves. Here we show that Scaptomyza flava larvae can also vector P. syringae to and from feeding sites, and that they not only feed more, but also develop faster on plants previously infected with P. syringae. Our genetic and physiological data show that P. syringae enhances S. flava feeding on infected plants at least in part by suppressing anti-herbivore defenses mediated by reactive oxygen species.

We present the first dated higher-level phylogenetic and biogeographic analysis of the butterfly family Riodinidae. This family is distributed worldwide, but more than 90% of the c. 1500 species are found in the Neotropics, while the c. 120 Old World species are concentrated in the Southeast Asian tropics, with minor Afrotropical and Australasian tropical radiations, and few temperate species. Morphologically based higher classification is partly unresolved, with genera incompletely assigned to tribes. Using 3666 bp from one mitochondrial and four nuclear markers for each of 23 outgroups and 178 riodinid taxa representing all subfamilies, tribes and subtribes, and 98 out of 145 described genera of riodinids, we estimate that Riodinidae split from Lycaenidae about 96 Mya in the mid-Cretaceous and started to diversify about 81 Mya. The Riodinidae are monophyletic and originated in the Neotropics, most likely in lowland proto-Amazonia. Neither the subfamily Euselasiinae nor the Nemeobiinae are monophyletic as currently constituted. The enigmatic, monotypic Neotropical genera Styx and Corrachia (most recently treated in Euselasiinae: Corrachiini) are highly supported as derived taxa in the Old World Nemeobiinae, with dispersal most likely occurring across the Beringia land bridge during the Oligocene. Styx and Corrachia, together with all other nemeobiines, are the only exclusively Primulaceae-feeding riodinids. The steadily increasing proliferation of the Neotropical Riodininae subfamily contrasts with the decrease in diversification in the Old World, and may provide insights into factors influencing the diversification rate of this relatively ancient clade of Neotropical insects. (C) 2015 Elsevier Inc. All rights reserved.

Erwinia tracheiphila is one of the most economically important pathogens of cucumbers, melons, squashes, pumpkins, and gourds in the northeastern and midwestern United States, yet its molecular pathology remains uninvestigated. Here, we report the first draft genome sequence of an E. tracheiphila strain isolated from an infected wild gourd (Cucurbita pepo subsp. texana) plant. The genome assembly consists of 7 contigs and includes a putative plasmid and at least 20 phage and prophage elements.

Mutualistic interactions typically involve the exchange of different commodities between species [1]. Nutritious secretions are produced by a number of insects and plants in exchange for services such as defense [2, 3]. These rewards are valuable metabolically and can be used to reinforce the behavior of symbiotic partners that can learn and remember them effectively [4, 5]. We show here novel effects of insect exocrine secretions produced by caterpillars in modulating the behavior of attendant ants in the food-for-defense interaction between lycaenid butterflies and ants [6]. Reward secretions from the dorsal nectary organ (DNO) of Narathura japonica caterpillars function to reduce the locomotory activities of their attendant ants, Pristomyrmex punctatus workers. Moreover, workers that feed from caterpillar secretions are significantly more likely to show aggressive responses to eversion of the tentacle organs of the caterpillars. Analysis of the neurogenic amines in the brains of workers that consumed caterpillar secretions showed a significant decrease in levels of dopamine compared with controls. Experimental treatments in which reserpine, a known inhibitor of dopamine in Drosophila, was fed to workers similarly reduced their locomotory activity. We conclude that DNO secretions of lycaenid caterpillars can manipulate attendant ant behavior by altering dopaminergic regulation and increasing partner fidelity. Unless manipulated ants also receive a net nutritional benefit from DNO secretions, this suggests that similar reward-for-defense interactions that have been traditionally considered to be mutualisms may in fact be parasitic in nature.

The biodiversity of tropical forests consists primarily of small organisms that are difficult to detect and characterize. Next-generation sequencing (NGS) methods can facilitate analyses of these arthropod and microbial communities, leading to a better understanding of existing diversity and factors influencing community assembly. The pitchers of carnivorous pitcher plants often house surprisingly discrete communities and provide ideal systems for analysis using an NGS approach. The plants digest insects in order to access essential nutrients while growing in poor soils; however, the pitchers are also home to communities of living organisms, called inquilines. Certain arthropods appear to have coevolved with their pitcher plant hosts and are not found in other environments. We used Illumina amplicon sequencing of 18S rDNA to characterize the eukaryotes in three species of Nepenthes (Nepenthaceae) pitcher plants – N. gracilis, N. rafflesiana and N. ampullaria – in each of three different parks in Singapore. The data reveal an unexpected diversity of eukaryotes, significant differences in community diversity among host species, variation in host specificity of inquilines and the presence of gregarine parasites. Counts of whole inquiline arthropods from the first collection year were roughly correlated with scaled 18S sequence abundances, indicating that amplicon sequencing is an effective means of gauging community structure. We barcoded a subset of the dipteran larvae using COI primers, and the resulting phylogenetic tree is mostly congruent with that found using the 18S locus, with the exception of one of five morphospecies. For many 18S and COI sequences, the best BLASTn matches showed low sequence identity, illustrating the need for better databases of Southeast Asian dipterans. Finally, networks of core arthropods and their host species were used to investigate degree of host specificity across multiple hosts, and this revealed significant specialization of certain arthropod fauna.

The Aphnaeinae (Lepidoptera: Lycaenidae) are a largely African subfamily of 278 described species that exhibit extraordinary life-history variation. The larvae of these butterflies typically form mutualistic associations with ants, and feed on a wide variety of plants, including 23 families in 19 orders. However, at least one species in each of 9 of the 17 genera is aphytophagous, parasitically feeding on the eggs, brood or regurgitations of ants. This diversity in diet and type of symbiotic association makes the phylogenetic relations of the Aphnaeinae of particular interest. A phylogenetic hypothesis for the Aphnaeinae was inferred from 4.4kb covering the mitochondrial marker COI and five nuclear markers (wg, H3, CAD, GAPDH and EF1) for each of 79 ingroup taxa representing 15 of the 17 currently recognized genera, as well as three outgroup taxa. Maximum Parsimony, Maximum Likelihood and Bayesian Inference analyses all support Heath's systematic revision of the clade based on morphological characters. Ancestral range inference suggests an African origin for the subfamily with a single dispersal into Asia. The common ancestor of the aphnaeines likely associated with myrmicine ants in the genus Crematogaster and plants of the order Fabales.

Of the four most diverse insect orders, Lepidoptera contains remarkably few predatory and parasitic species. Although species with these habits have evolved multiple times in moths and butterflies, they have rarely been associated with diversification. The wholly aphytophagous subfamily Miletinae (Lycaenidae) is an exception, consisting of nearly 190 species distributed primarily throughout the Old World tropics and subtropics. Most miletines eat Hemiptera, although some consume ant brood or are fed by ant trophallaxis. A well-resolved phylogeny inferred using 4915 bp from seven markers sampled from representatives of all genera and nearly one-third the described species was used to examine the biogeography and evolution of biotic associations in this group. Biogeographic analyses indicate that Miletinae likely diverged from an African ancestor near the start of the Eocene, and four lineages dispersed between Africa and Asia. Phylogenetic constraint in prey selection is apparent at two levels: related miletine species are more likely to feed on related Hemiptera, and related miletines are more likely to associate with related ants, either directly by eating the ants, or indirectly by eating hemipteran prey that are attended by those ants. These results suggest that adaptations for host ant location by ovipositing female miletines may have been retained from phytophagous ancestors that associated with ants mutualistically.