Publications by EEOB faculty April 1 - April 30

May 1, 2017
eeob 2016

The Phanuromyia galeata species group (Hymenoptera, Platygastridae, Telenominae): shining a lantern into an unexplored corner of Neotropical diversity

Katherine C. Nesheim, Lubomír Masner, Norman F. Johnson. 2017. ZooKeys 663: 71-105 


The Phanuromyia galeata species group is delineated and its species richness explored for the first time (Hymenoptera: Platygastridae, Telenominae). Fifteen species are described, all of which are new: Phanuromyia comata Nesheim & Masner, sp. n. (Brazil), P. constellata Nesheim, sp. n. (Paraguay), P. corys Nesheim & Masner, sp. n. (Brazil), P. cranos Nesheim & Masner, sp. n. (Bolivia, Costa Rica, Ecuador, French Guiana), P. cudo Nesheim & Masner, sp. n. (Belize, Bolivia, Brazil, Colombia, Costa Rica, Ecuador, French Guiana, Panama, Peru, Trinidad and Tobago, Venezuela), P. dissidens Nesheim & Masner, sp. n. (Bolivia, Brazil, French Guiana), P. galeata Nesheim & Masner, sp. n. (Belize, Brazil, Colombia, Costa Rica, Ecuador, El Salvador, French Guiana, Mexico, Peru), P. galerita Nesheim & Masner, sp. n. (Brazil, Ecuador, French Guiana), P. hjalmr Nesheim, sp. n. (Bolivia, Costa Rica, Ecuador, Paraguay, Venezuela), P. krossotos Nesheim, sp. n. (Ecuador), P. odo Nesheim, sp. n. (Belize, Bolivia, Brazil, Colombia, Costa Rica, Ecuador, El Salvador, French Guiana, Guatemala, Mexico, Panama, Peru, Trinidad and Tobago, Venezuela), P. pauper Nesheim, sp. n. (Ecuador, Peru), P. princeps Nesheim, sp. n. (Brazil, Ecuador, French Guiana), P. tonsura Nesheim, sp. n. (Brazil, Colombia, Ecuador, Paraguay, Peru), P. tubulifer Nesheim & Masner, sp. n. (Brazil, Guyana).

All roads lead to weediness: Patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza

Zhongyun Huang, Nelson D. Young, Michael Reagon, Katie E. Hyma, Kenneth M. Olsen, Yulin Jia, Ana L. Caicedo. 2017. Mol Ecol. DOI: 10.1111/mec.14120


Weedy rice (Oryza spp.), a weedy relative of cultivated rice (O. sativa), infests and persists in cultivated rice fields worldwide. Many weedy rice populations have evolved similar adaptive traits, considered part of the ‘agricultural weed syndrome’, making this an ideal model to study the genetic basis of parallel evolution. Understanding parallel evolution hinges on accurate knowledge of the genetic background and origins of existing weedy rice groups. Using population structure analyses of South Asian and US weedy rice, we show that weeds in South Asia have highly heterogeneous genetic backgrounds, with ancestry contributions both from cultivated varieties (aus and indica) and wild rice. Moreover, the two main groups of weedy rice in the USA, which are also related to aus and indica cultivars, constitute a separate origin from that of Asian weeds. Weedy rice populations in South Asia largely converge on presence of red pericarps and awns and on ease of shattering. Genomewide divergence scans between weed groups from the USA and South Asia, and their crop relatives are enriched for loci involved in metabolic processes. Some candidate genes related to iconic weedy traits and competitiveness are highly divergent between some weed-crop pairs, but are not shared among all weed-crop comparisons. Our results show that weedy rice is an extreme example of recurrent evolution, and suggest that most populations are evolving their weedy traits through different genetic mechanisms.

Do models parameterized with observations from the system predict larval yellow perch (Perca flavescens) growth performance better in Lake Erie?

Jose R. Marin Jarrin, Timothy B Johnson, Stuart A. Ludsin, Julie M Reichert, Kevin L Pangle. 2017. Canadian Journal of Fisheries and Aquatic Sciences, 10.1139/cjfas-2016-0392


Growth performance can influence survival during early life. As such, a range of statistical to mechanistic modeling approaches has been used to predict growth performance, with few studies evaluating prediction accuracy. We tested the ability of three models to estimate observed larval yellow perch (Perca flavescens) growth and length in western Lake Erie (USA-Canada). We found that a General Linear Model developed using yellow perch data from western Lake Erie performed best, followed closely by a semi-mechanistic Individual-Based Model (IBM) specific to Lake Erie yellow perch and worst by a General multi-species IBM. We suspect the Statistical Model performed better because, unlike IBMs, it does not require prey availability data, probably poorly represented by zooplankton samples, and because the IBMs are imperfectly parameterized. Our findings indicate that caution should be exercised when using general IBMs given that the models parameterized with observations from the system of interest outperformed the general IBM in providing accurate fish growth and length estimates, pointing to the need for research that can improve existing mechanism-based models of larval growth.

Strong spatial-genetic congruence between a wood-feeding cockroach and its bacterial endosymbiont, across a topographically complex landscape

Ryan C. Garrick, Zakee L. Sabree, Benjamin C. Jahnes, Jeffrey C. Oliver. 2017. Journal of Biogeography. DOI: 10.1111/jbi.12992


Our overarching finding of strong congruence is reflected by broader-scale cophylogenetic studies of related Cryptocercus and Blattabacterium taxa. Accordingly, we suggest that members of this symbiosis may provide an excellent opportunity for investigating geographic scaling of processes that affect biogeographic patterns. However, fine-scale sampling coupled with geospatial analyses detected rare and/or minor discordances that appeared to be localized within the most deeply dissected topographic regions of the southern Appalachian Mountains, and these warrant further exploration.

Contrasting abundance and contribution of clonal proliferation to the population structure of the corkscrew sea anemone Bartholomea annulata in the tropical Western Atlantic

Benjamin M. Titus, Marymegan Daly, Jason Macrander, Annelise Del Rio, Scott R. Santos, Nanette E. Chadwick. 2017. Invertebrate Biology 136(1): 62–74. DOI: 10.1111/ivb.12162


Clonal propagation is an important life history trait for many sessile organisms, and often leads to the formation of monoclonal aggregations. In the marine environment, sea anemones have been model species for testing theory regarding the evolution of sex and understanding the contribution of sexual versus asexual reproduction to the population structure in facultatively clonal animals. However, little attention has been paid to tropical actiniarians. The corkscrew anemone Bartholomea annulata is common in tropical marine habitats in the western Atlantic and Caribbean; it forms small aggregations (2–4 anemones) on coral reefs and larger aggregations (>10 anemones) in mangrove habitats. We used field surveys and molecular analyses to investigate patterns of distribution, abundance, and genetic structure of aggregations formed by B. annulata on a reef in the US Virgin Islands and in a unique mangrove habitat in the Florida Keys. Abundance was greatest at the abandoned rock quarry mangrove habitat in the Florida Keys, where anemones formed continuously distributed aggregations carpeting the exposed limestone walls. Genetic diversity assessed via intersimple sequence repeats (ISSRs) and six microsatellite loci revealed that asexual reproduction plays only a minor role in the formation of both small and large anemone aggregations. Specifically, ISSR analyses showed that only ~10% of anemone
aggregations were clonal in the US Virgin Islands, while microsatellite genotyping identified clonality in only 1 of 35 aggregations. In the Florida Keys, only four clonal genotypes were recovered within aggregations, but eight clones, representing 33% of the total surveyed population, had individuals in multiple aggregations. Thus, population structure of B. annulata appears to rely primarily on sexual reproduction, although asexual reproduction may play a nontrivial role in some environments. Mechanisms that drive the formation of genotypically diverse aggregations remain unknown, but may include attraction toward conspecifics, shared use of preferred habitats, or the local retention of larvae in partially enclosed habitats.

Comparing the utility of host and primary endosymbiont loci for predicting global invasive insect genetic structuring and migration patterns

Alejandro Otero-Bravo, Zakee L. Sabree. 2017. Biological Control.


Halyomorpha halys, commonly known as the Brown Marmorated Stinkbug, is a highly polyphagous invasive pest introduced from East Asia into North America and Europe. It harbors ‘Candidatus Pantoea carbekii’, an obligately-associated, vertically-inherited gamma-proteobacterial mutualist. We evaluated the use of this symbiont as a proxy for measuring host diversity, distribution, and phylogeography. Despite the symbiont’s accelerated molecular evolution, the symbiont genome shows relatively lower genetic diversity and structuring compared to the host mitochondrial genome in both native and invaded ranges. Therefore, we conclude that P. carbekii is not as effective as the host mitochondria for determining recent host population history and migration.

Do ecological communities disperse across biogeographic barriers as a unit?

Jordan D. Satler, Bryan C. Carstens. 2017. Molecular Ecology. DOI: 10.1111/mec.14137


Biogeographic barriers have long been implicated as drivers of biological diversification, but how these barriers influence co-occurring taxa can vary depending on factors intrinsic to the organism and in their relationships with other species. Due to the interdependence among taxa, ecological communities present a compelling opportunity to explore how interactions among species may lead to a shared response to historical events. Here we collect single nucleotide polymorphism data from five commensal arthropods associated with the Sarracenia alata carnivorous pitcher plant, and test for codiversification across the Mississippi River, a major biogeographic barrier in the southeastern United States. Population genetic structure in three of the ecologically dependent arthropods mirrors that of the host pitcher plant, with divergence time estimates suggesting two of the species (the pitcher plant moth Exyra semicrocea and a flesh fly Sarcophaga sarraceniae) dispersed synchronously across this barrier along with the pitcher plant. Patterns in population size and genetic diversity suggest the plant and ecologically dependent arthropods dispersed from east to west across the Mississippi River. In contrast, species less dependent on the plant ecologically show discordant phylogeographic patterns. This study demonstrates that ecological relationships may be an important predictor of codiversification, and supports recent suggestions that organismal trait data should be prominently featured in comparative phylogeographic investigations.

Self-compatibility is over-represented on islands

Dena L. Grossenbacher, Yaniv Brandvain, Josh R. Auld, Martin Burd, Pierre-Olivier Cheptou, Jeffrey K. Conner, Alannie G. Grant, Stephen M. Hovick, John R. Pannell, Anton Pauw, Theodora Petanidou, April M. Randle, Rafael Rubio de Casas, Jana Vamosi, Alice Winn, Boris Igic, Jeremiah W. Busch, Susan Kalisz, Emma E. Goldberg. 2017. New Phytologist. DOI: 10.1111/nph.14534


Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker's law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families.

Effects of over-expressing a native gene encoding 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) on glyphosate resistance in Arabidopsis thaliana

Xiao Yang , Zachery T. Beres, Lin Jin, Jason T. Parrish, Wanying Zhao, David Mackey, Allison A. Snow. 2017. PLOS


Widespread overuse of the herbicide glyphosate, the active ingredient in RoundUp®, has led to the evolution of glyphosate-resistant weed biotypes, some of which persist by overproducing the herbicide’s target enzyme, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS). EPSPS is a key enzyme in the shikimic acid pathway for biosynthesis of aromatic amino acids, lignin, and defensive compounds, but little is known about how overproducing EPSPS affects downstream metabolites, growth, or lifetime fitness in the absence of glyphosate. We are using Arabidopsis as a model system for investigating phenotypic effects of overproducing EPSPS, thereby avoiding confounding effects of genetic background or other mechanisms of herbicide resistance in agricultural weeds. Here, we report results from the first stage of this project. We designed a binary vector expressing a native EPSPS gene from Arabidopsis under control of the CaMV35S promoter (labelled OX, for over-expression). For both OX and the empty vector (labelled EV), we obtained nine independent T3 lines. Subsets of these lines were used to characterize glyphosate resistance in greenhouse experiments. Seven of the nine OX lines exhibited enhanced glyphosate resistance when compared to EV and wild-type control lines, and one of these was discarded due to severe deformities. The remaining six OX lines exhibited enhanced EPSPS gene expression and glyphosate resistance compared to controls. Glyphosate resistance was correlated with the degree of EPSPS over-expression for both vegetative and flowering plants, indicating that glyphosate resistance can be used as a surrogate for EPSPS expression levels in this system. These findings set the stage for examination of the effects of EPSPS over-expression on fitness-related traits in the absence of glyphosate. We invite other investigators to contact us if they wish to study gene expression, downstream metabolic effects, and other questions with these particular lines.

Comparative behavioural observations demonstrate the ‘cleaner’ shrimp Periclimenes yucatanicus engages in true symbiotic cleaning interactions

Benjamin M. Titus, Clayton Vondriska, Marymegan Daly. 2017. Royal Society of Open Science. DOI: 10.1098/rsos.170078


Cleaner shrimps are ecologically important members of coral reef communities, but for many species, cleaner status (i.e. dedicated, facultative and mimic), clientele and ecological role remain unverified or described. On Caribbean coral reefs, the spotted ‘cleaner’ shrimp Periclimenes yucatanicus forms symbioses with sea anemones that may serve as cleaning stations for reef fishes. The status of this species as a cleaner is ambiguous: only a single in situ cleaning interaction has been reported, and in the only test of its efficacy as a cleaner, it did not effectively reduce parasite loads from surgeonfish. It has subsequently been hypothesized by other authors to be a cleaner mimic. We conduct a comparative investigation of cleaning behaviour between P. yucatanicus and the ecologically similar, closely related, dedicated cleaner shrimp Ancylomenes pedersoni in Curacao, Netherlands Antilles. We provide the first detailed field observations on cleaning behaviour for P. yucatanicus and test multiple behavioural expectations surrounding mimicry in cleaning symbioses. We found that P. yucatanicus regularly signals its availability to clean, client fishes visit regularly and the shrimp does engage in true symbiotic cleaning interactions, but these are brief and our video reflects a species that appears hesitant to engage posing clients. In comparison to A. pedersoni, P. yucatanicus stations had significantly fewer total visits and cleans, and 50% of all cleaning interactions at P. yucatanicus stations were shorter than 10 s in total duration. Our behavioural observations confirm that P. yucatanicus is a true cleaner shrimp; we reject the hypothesis of mimicry. However, investigation is needed to confirm whether this species is a dedicated or facultative cleaner. We hypothesize that P. yucatanicus has a specialized ecological role as a cleaner species, compared to A. pedersoni.

Anthopleura and the phylogeny of Actinioidea (Cnidaria: Anthozoa: Actiniaria)

M. Daly, L. M. Crowley, P. Larson, E. Rodríguez, E. Heestand Saucier, D. G. Fautin. 2017. Organisms Diversity & Evolution. doi:10.1007/s13127-017-0326-6


Members of the sea anemone genus Anthopleura are familiar constituents of rocky intertidal communities. Despite its familiarity and the number of studies that use its members to understand ecological or biological phenomena, the diversity and phylogeny of this group are poorly understood. Many of the taxonomic and phylogenetic problems stem from problems with the documentation and interpretation of acrorhagi and verrucae, the two features that are used to recognize members of Anthopleura. These anatomical features have a broad distribution within the superfamily Actinioidea, and their occurrence and exclusivity are not clear. We use DNA sequences from the nucleus and mitochondrion and cladistic analysis of verrucae and acrorhagi to test the monophyly of Anthopleura and to evaluate the pattern of distribution of acrorhagi and verrucae. We find that Anthopleura is paraphyletic: although species of the genus cluster together, some groups also include members of genera like Bunodosoma, Aulactinia, Oulactis, and Actinia. This paraphyly is explained in part by the discovery that acrorhagi and verrucae are pleisiomorphic for the subset of Actinioidea studied.