Publications by EEOB faculty May 1 - May 31

May 23, 2016
EEOB graphic 2016

Cryobiology of the freeze-tolerent gall fly Eurosta solidaginis: overwintering energetics and heat shock proteins

Lee, Richard E., Dommel, Robyn A., Joplin, Karl H., Denlinger, David L. 2016. Clim. Res, 5, 61-67.


The goldenrod gall fly E urosta solidaginis (Diptera: Tephritidae) ranges from the southern us. northward into Canada. The larva overwinters within a ball gall on the stem of goldenrod Solidago spp. The galls often extend above the snowpack, exposing the larva to a wide range of environmental extremes in winter. This species has received extensive attention as a freeze-tolerant insect model. A seasonal study of the overwintering bioenergetics of an Ohio, USA population revealed marked decreased in body weight, lipid and total caloric content in October and November, when environmental temperatures were the highest. Overwintering larvae produce heat shock proteins in responses to high temperature exposure. However, unlike other insects E. solidagnis does not appear to synthesize heat shock proteins in response to low-temperature exposure.

Relative Performance of Non-Local Cultivars and Local, Wild Populations of Switchgrass (Panicum virgatum) in Competition Experiments

D. J. Palik , A. A. Snow, A. L. Stottlemyer, M. N. Miriti, E. A. Heaton. 2016.


The possibility of increased invasiveness in cultivated varieties of native perennial species is a question of interest in biofuel risk assessment. Competitive success is a key factor in the fitness and invasive potential of perennial plants, and thus the large-scale release of high-yielding biomass cultivars warrants empirical comparisons with local conspecifics in the presence of competitors. We evaluated the performance of non-local cultivars and local wild biotypes of the tallgrass species Panicum virgatum L. (switchgrass) in competition experiments during two growing seasons in Ohio and Iowa. At each location, we measured growth and reproductive traits (plant height, tiller number, flowering time, aboveground biomass, and seed production) of four non-locally sourced cultivars and two locally collected wild biotypes. Plants were grown in common garden experiments under three types of competition, referred to as none, moderate (with Schizachyrium scoparium), and high (with Bromus inermis). In both states, the two “lowland” cultivars grew taller, flowered later, and produced between 2x and 7.5x more biomass and between 3x and 34x more seeds per plant than local wild biotypes, while the other two cultivars were comparable to wild biotypes in these traits. Competition did not affect relative differences among biotypes, with the exception of shoot number, which was more similar among biotypes under high competition. Insights into functional differences between cultivars and wild biotypes are crucial for developing biomass crops while mitigating the potential for invasiveness. Here, two of the four cultivars generally performed better than wild biotypes, indicating that these biotypes may pose more of a risk in terms of their ability to establish vigorous feral populations in new regions outside of their area of origin. Our results support an ongoing assessment of switchgrass cultivars developed for large-scale planting for biofuels.

Population Structure in the Model Grass Brachypodium distachyon Is Highly Correlated with Flowering Differences across Broad Geographic Areas.

Tyler, L., S. J. Lee, N. D. Young, G. A. DeIulio, E. Benavente, M. Reagon, J. Sysopha, R. M. Baldini, A. Troìa, S. P. Hazen, and A. L. Caicedo. 2016.  Plant Genome 0. doi:10.3835/plantgenome2015.08.0074


The small, annual grass Brachypodium distachyon (L.) Beauv., a close relative of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.), is a powerful model system for cereals and bioenergy grasses. Genome-wide association studies (GWAS) of natural variation can elucidate the genetic basis of complex traits but have been so far limited in B. distachyon by the lack of large numbers of well-characterized and sufficiently diverse accessions. Here, we report on genotyping-by-sequencing (GBS) of 84 B. distachyon, seven B. hybridum, and three B. stacei accessions with diverse geographic origins including Albania, Armenia, Georgia, Italy, Spain, and Turkey. Over 90,000 high-quality single-nucleotide polymorphisms (SNPs) distributed across the Bd21 reference genome were identified. Our results confirm the hybrid nature of the B. hybridum genome, which appears as a mosaic of B. distachyon-like and B. stacei-like sequences. Analysis of more than 50,000 SNPs for the B. distachyon accessions revealed three distinct, genetically defined populations. Surprisingly, these genomic profiles are associated with differences in flowering time rather than with broad geographic origin. High levels of differentiation in loci associated with floral development support the differences in flowering phenology between B. distachyon populations. Genome-wide association studies combining genotypic and phenotypic data also suggest the presence of one or more photoperiodism, circadian clock, and vernalization genes in loci associated with flowering time variation within B. distachyon populations. Our characterization elucidates genes underlying population differences, expands the germplasm resources available for Brachypodium, and illustrates the feasibility and limitations of GWAS in this model grass.

Comparative Transcriptomics Reveals Key Gene Expression Differences between Diapausing and Non-Diapausing Adults of Culex pipiens.

Kang DS, Cotten MA, Denlinger DL, Sim C. 2016. PLoS ONE 11(4): e0154892. doi:10.1371/journal.pone.0154892


As a vector of West Nile virus and other human pathogens, the mosquito Culex pipiens is of growing concern in the US [1–4]. Members of the Culex pipiens complex of mosquitoes are virtually indistinguishable by simple morphometrics, yet they exhibit a robust range of life strategies driven by genetic architecture [5, 6]. Among members of this complex, only Culex pipiens form pipiens undergoes an overwintering diapause, a feature that is critical for expanding its habitat to temperate regions.
Diapause is an alternative developmental program in which the mosquito senses impending changes in its environment and adapts accordingly by entering a dormant state [7, 8]. Diapause is an anticipated response triggered by shortened day lengths and low temperature, which in turn restrict insulin signal and consequently halt the release of the isoprenoid juvenile hormone [9, 10]. This absence of juvenile hormone induces a phenotype with diverse physiological, developmental and behavioral traits including the seeking of protected overwintering sites, delayed reproductive development, stress tolerance, sugar gluttony and nutrient rationing. The adult diapause of Cx.pipiens is initiated only in females, and the programming begins during the larval and pupal stages. Post-eclosion these females will mate, but will not engage in hematophagous (blood feeding) behavior or vitellogenesis (egg yolk deposition) until termination of the diapause program [8]. These responses allow the mosquito to prepare for winter, conserve energy reserves and avoid adverse conditions. Diapause is thus a critical adaptation for survival of these vectors of human and animal disease. Despite the crucial role of diapause to mosquito survival, we know little about how mosquitoes are able translate complex environmental signals into the developmental switch that evokes the complex hormonal and physiological traits that comprise the diapause syndrome [10–18].
Diapause is a quantitative trait in which multiple genes share complex interactions that generate the phenotype. Genome wide interactions underlying this trait have been previously investigated in a variety of organisms including bumble bees, crickets, spider mites, flesh flies, apple maggots, moths, house flies and other mosquitoes [19–27]. In Cx. pipiens, several minor QTLs and a major QTL have been identified, but mapping studies have been impeded by a lack of markers [28]. Here we use RNA-seq to simultaneously quantify and identify transcriptional profiles of diapausing and non-diapausing females of Cx. pipiens to generate hypotheses that may explain the dramatic differences in these two phenotypes.

No safety in the trees: Local and species-level adaptation of an arboreal squirrel to the venom of sympatric rattlesnakes

Abby M. Pomento1, Blair W. Perry1, Robert D. Denton, H. Lisle Gibbs, Matthew L. Holding. 2016. doi:10.1016/j.toxicon.2016.05.003


Within some species, squirrels respond to variable selection from venomous snake predators by showing population-level variation in resistance, while between species, some rattlesnakes possess venom that is more effective at overcoming venom resistance in different species of squirrels. A functional evaluation of resistance variation to venom within and between species of squirrels and snakes can link resistance variation to its evolutionary causes across these different evolutionary scales. To do this, we compared the effectiveness of squirrel sera in inhibiting rattlesnake (Crotalus spp.) venom metalloproteinase activity between populations and between species to test for a response to local variation in selection from a single rattlesnake predator and for specialization of two resistant squirrel species to each of their distinct sympatric snake predators. We found that Timber Rattlesnake (Crotalus horridus) venom inhibition by Eastern gray squirrels (Sciurus carolinensis) is higher at a site where the rattlesnakes are present, which suggests selection may maintain venom resistance in populations separated by short distances. Next, we performed a reciprocal cross of venoms and sera from two rattlesnake and two squirrel species. This showed that squirrel resistance is lower when tested against venom from allopatric compared to sympatric rattlesnake species, demonstrating that squirrel inhibitors are specialized to sympatric venom and suggesting a tradeoff in terms of specialization to the venom of a specific species of rattlesnake predator. This pattern can be explained if inhibitors must recognize venom proteins and resistance evolution tracks venom evolution.

Demographic consequences of greater clonal than sexual reproduction in Dicentra canadensis.

Lin, C.-H., Miriti, M. N. and Goodell, K. 2016. Ecol Evol. doi:10.1002/ece3.2163


Clonality is a widespread life history trait in flowering plants that may be essential for population persistence, especially in environments where sexual reproduction is unpredictable. Frequent clonal reproduction, however, could hinder sexual reproduction by spatially aggregating ramets that compete with seedlings and reduce inter-genet pollination. Nevertheless, the role of clonality in relation to variable sexual reproduction in population dynamics is often overlooked. We combined population matrix models and pollination experiments to compare the demographic contributions of clonal and sexual reproduction in three Dicentra canadensis populations, one in a well-forested landscape and two in isolated forest remnants. We constructed stage-based transition matrices from 3 years of census data to evaluate annual population growth rates, λ. We used loop analysis to evaluate the relative contribution of different reproductive pathways to λ. Despite strong temporal and spatial variation in seed set, populations generally showed stable growth rates. Although we detected some pollen limitation of seed set, manipulative pollination treatments did not affect population growth rates. Clonal reproduction contributed significantly more than sexual reproduction to population growth in the forest remnants. Only at the well-forested site did sexual reproduction contribute as much as clonal reproduction to population growth. Flowering plants were more likely to transition to a smaller size class with reduced reproductive potential in the following year than similarly sized nonflowering plants, suggesting energy trade-offs between sexual and clonal reproduction at the individual level. Seed production had negligible effects on growth and tuber production of individual plants. Our results demonstrate that clonal reproduction is vital for population persistence in a system where sexual reproduction is unpredictable. The bias toward clonality may be driven by low fitness returns for resource investment in sexual reproduction at the individual level. However, chronic failure in sexual reproduction may exacerbate the imbalance between sexual and clonal reproduction and eventually lead to irreversible loss of sex in the population.

Symbiotic essential amino acids provisioning in the American cockroach, Periplaneta americana (Linnaeus) under various dietary conditions. 

Ayayee PA, Larsen T, Sabree Z. 2016. PeerJ 4:e2046
Insect gut microbes have been shown to provide nutrients such as essential amino acids (EAAs) to their hosts. How this symbiotic nutrient provisioning tracks with the host’s demand is not well understood. In this study, we investigated microbial essential amino acid (EAA) provisioning in omnivorous American cockroaches (Periplaneta americana), fed low-quality (LQD) and comparatively higher-quality dog food (DF) diets using carbon stable isotope ratios of EAAs (δ13CEAA). We assessed non-dietary EAA input, quantified as isotopic offsets (Δ13C) between cockroach (δ13CCockroach EAA) and dietary (δ13CDietary EAA) EAAs, and subsequently determined biosynthetic origins of non-dietary EAAs in cockroaches using 13C-fingerprinting with dietary and representative bacterial and fungal δ13CEAA. Investigation of biosynthetic origins of de novo non-dietary EAAs indicated bacterial origins of EAA in cockroach appendage samples, and a mixture of fungal and bacterial EAA origins in gut filtrate samples for both LQD and DF-fed groups. We attribute the bacteria-derived EAAs in cockroach appendages to provisioning by the fat body residing obligate endosymbiont, Blattabacterium and gut-residing bacteria. The mixed signatures of gut filtrate samples are attributed to the presence of unassimilated dietary, as well as gut microbial (bacterial and fungal) EAAs. This study highlights the potential impacts of dietary quality on symbiotic EAA provisioning and the need for further studies investigating the interplay between host EAA demands, host dietary quality and symbiotic EAA provisioning in response to dietary sufficiency or deficiency.

Testing the skill of numerical hydraulic modeling to simulate spatiotemporal flooding patterns in the Logone floodplain, Cameroon

Alfonso Fernández, Mohammad Reza Najafi, Michael Durand, Bryan G. Mark, Mark Moritz, Hahn Chul Jung, Jeffrey Neal, Apoorva Shastry, Sarah Laborde, Sui Chang Phang, Ian M. Hamilton, Ningchuan Xiao. 2016. doi:10.1016/j.jhydrol.2016.05.026


Recent innovations in hydraulic modeling have enabled global simulation of rivers, including simulation of their coupled wetlands and floodplains. Accurate simulations of floodplains using these approaches may imply tremendous advances in global hydrologic studies and in biogeochemical cycling. One such innovation is to explicitly treat sub-grid channels within two-dimensional models, given only remotely sensed data in areas with limited data availability. However, predicting inundated area in floodplains using a sub-grid model has not been rigorously validated. In this study, we apply the LISFLOOD-FP hydraulic model using a sub-grid channel parameterization to simulate inundation dynamics on the Logone River floodplain, in northern Cameroon, from 2001 to 2007. Our goal was to determine whether floodplain dynamics could be simulated with sufficient accuracy to understand human and natural contributions to current and future inundation patterns. Model inputs in this data-sparse region include in situ river discharge, satellite-derived rainfall, and the shuttle radar topography mission (SRTM) floodplain elevation. We found that the model accurately simulated total floodplain inundation, with a Pearson correlation coefficient greater than 0.9, and RMSE less than 700 km2, compared to peak inundation greater than 6,000 km2. Predicted discharge downstream of the floodplain matched measurements (Nash-Sutcliffe efficiency of 0.81), and indicated that net flow from the channel to the floodplain was modeled accurately. However, the spatial pattern of inundation was not well simulated, apparently due to uncertainties in SRTM elevations. We evaluated model results at 250, 500 and 1000-m spatial resolutions, and found that results are insensitive to spatial resolution. We also compared the model output against results from run of LISFLOOD-FP in which the sub-grid channel parameterization was disabled, finding that the sub-grid parameterization simulated more realistic dynamics. These results suggest that analysis of global inundation is feasible using a sub-grid model, but that spatial patterns at sub-kilometer resolutions still needs to be adequately predicted.

A perspective on needed research, modeling, and management approaches that can enhance Great Lakes fisheries management under changing ecosystem conditions

Kristen M. DeVanna Fussell, Ralph E.H. Smith, Michael E. Fraker, Leon Boegman, Kenneth T. Frank, Thomas J. Miller, Jeff T. Tyson, Kristin K. Arend, Daniel Boisclairh, Stephanie J. Guildfordi, Robert E. Heckyi, Tomas O. Hӧӧk, Olaf P. Jensen, Joel K. Llopiz, Cassandra J. May, Raymond G. Najjar, Lars G. Rudstam, Christopher T. Taggart, Yerubandi R. Rao, Stuart A. Ludsin. 2016. Journal of Great Lakes Research. doi:10.1016/j.jglr.2016.04.007
The Great Lakes Fishery Commission sponsored a 2-day workshop that sought to enhance the ability of Great Lakes agencies to understand, predict, and ideally manage fisheries production in the face of changes in natural and anthropogenic forcings (e.g., climate, invasive species, and nutrients). The workshop brought together 18 marine and freshwater researchers with collective expertise in aquatic ecology, physical oceanography, limnology, climate modeling, and ecosystem modeling, and two individuals with fisheries management expertise. We report on the outcome of a writing exercise undertaken as part of this workshop that challenged each participant to identify three needs, which if addressed, could most improve the ability of Great Lakes agencies to manage their fisheries in the face of ecosystem change. Participant responses fell into two categories. The first identified gaps in ecological understanding, including how physical and biological processes can regulate early life growth and survival, how life-history strategies vary across species and within populations, and how anthropogenic stressors (e.g., nutrient runoff, climate change) can interact to influence fish populations. The second category pointed to the need for improved approaches to research (e.g., meta-analytic, comparative, spatial translation) and management (e.g., mechanistic management models, consideration of multi-stock management), and also identified the need for improved predictive models of the physical environment and associated ecosystem monitoring programs. While some progress has been made toward addressing these needs, we believe that a continued focus will be necessary to enable optimal fisheries management responses to forthcoming ecosystem change.