Publications by EEOB faculty August 6 - September 5

September 4, 2014

Proteomic and toxicological profiling of the venom of Bothrocophias campbelli, a pitviper species from Ecuador and Colombia

David Salazar-Valenzuela, Diana Mora-Obando, María Laura Fernández, Amaru Loaiza-Lange, H. Lisle Gibbs, Bruno Lomonte. Toxicon, 90:15–25. DOI: 10.1016/j.toxicon.2014.07.012


Detailed snake venom proteomes for nearly a hundred species in different pitviper genera have accumulated using ‘venomics’ methodologies. However, venom composition for some lineages remains poorly known. Bothrocophias (toad-headed pitvipers) is a genus restricted to the northwestern portion of South America for which information on venom composition is lacking. Here, we describe the protein composition, toxicological profiling, and antivenom neutralization of the venom of Bothrocophias campbelli, a species distributed in Colombia and Ecuador. Our analyses show that its venom mainly consists of phospholipases A2 (43.1%), serine proteinases (21.3%), and metalloproteinases (15.8%). The low proportion of metalloproteinases and high amount of a Lys49 phospholipase A2 homologue correlate well with the low hemorrhagic and high myotoxic effects found. Overall, B. campbelli venom showed a simpler composition compared to other crotalines in the region. A polyvalent antivenom prepared with a mixture of Bothrops asper, Crotalus simus, and Lachesis stenophrys venoms cross-recognized B. campbelli venom and neutralized its lethal effect in mice, albeit with a lower potency than for B. asper venom. Additional work comparing B. campbelli venom properties with those of related species could help understand the evolution of different venom protein families during the South American radiation of New World pitvipers.

Gibbs Lab

A comprehensive approach to evaluating watershed models for predicting river flow regimes critical to downstream ecosystem services

Seyoum Y. Gebremariam, Jay F. Martin, Carlo DeMarchi, Nathan S. Bosch, Remegio Confesor, Stuart A. Ludsin. Environmental Modelling & Software.Volume 61, November 2014, Pages 121–134. DOI: 10.1016/j.envsoft.2014.07.004


Selection of strategies that help reduce riverine inputs requires numerical models that accurately quantify hydrologic processes. While numerous models exist, information on how to evaluate and select the most robust models is limited. Toward this end, we developed a comprehensive approach that helps evaluate watershed models in their ability to simulate flow regimes critical to downstream ecosystem services. We demonstrated the method using the Soil and Water Assessment Tool (SWAT), the Hydrological Simulation Program–FORTRAN (HSPF) model, and Distributed Large Basin Runoff Model (DLBRM) applied to the Maumee River Basin (USA). The approach helped in identifying that each model simulated flows within acceptable ranges. However, each was limited in its ability to simulate flows triggered by extreme weather events, owing to algorithms not being optimized for such events and mismatched physiographic watershed conditions. Ultimately, we found HSPF to best predict river flow, whereas SWAT offered the most flexibility for evaluating agricultural management practices.

Ludsin Lab

Time flies: Time of day and social environment affect cuticular hydrocarbon sexual displays in Drosophila serrata
Gershman, Susan N.; Toumishey, Ethan; Rundle, Howard D.

Recent work on Drosophila cuticular hydrocarbons (CHCs) challenges a historical assumption that CHCs in flies are largely invariant. Here we examine the effect of time of day and social environment on a suite of sexually selected CHCs in Drosophila serrata. We demonstrate that males become more attractive to females during the time of day that flies are most active and when most matings occur, but females become less attractive to males during the same time of day. These opposing temporal changes may reflect differences in selection among the sexes. To evaluate the effect of social environment on male CHC attractiveness, we manipulated male opportunity for mating: male flies were housed either alone, with five females, with five males, or with five males and five females. We found that males had the most attractive CHCs when with females, and less attractive CHCs when with competitor males. Social environment mediated how male CHC attractiveness cycled: males housed with females and/or other males showed temporal changes in CHC attractiveness, whereas males housed alone did not. In total, our results demonstrate temporal patterning of male CHCs that is dependent on social environment, and suggest that such changes may be beneficial to males.

Gershman Lab

Compact genome of the Antarctic midge is likely an adaptation to an extreme environment
Joanna L. Kelley, Justin T. Peyton, Anna-Sophie Fiston-Lavier, Nicholas M. Teets, Muh-Ching Yee, J. Spencer Johnston, Carlos D. Bustamante, Richard E. Lee, David L. Denlinger. Nature Communications. doi:10.1038/ncomms5611

The midge, Belgica antarctica, is the only insect endemic to Antarctica, and thus it offers a powerful model for probing responses to extreme temperatures, freeze tolerance, dehydration, osmotic stress, ultraviolet radiation and other forms of environmental stress. Here we present the first genome assembly of an extremophile, the first dipteran in the family Chironomidae, and the first Antarctic eukaryote to be sequenced. At 99 megabases, B. antarctica has the smallest insect genome sequenced thus far. Although it has a similar number of genes as other Diptera, the midge genome has very low repeat density and a reduction in intron length. Environmental extremes appear to constrain genome architecture, not gene content. The few transposable elements present are mainly ancient, inactive retroelements. An abundance of genes associated with development, regulation of metabolism and responses to external stimuli may reflect adaptations for surviving in this harsh environment.

Denlinger Lab

A comparative study of an innate immune response in Lamprologine cichlid fishes

Constance M. O’Connor, Adam R. Reddon, Susan E. Marsh-Rollo, Jennifer K. Hellmann, Isaac Y. Ligocki, Ian M. Hamilton, Sigal Balshine.



Social interactions facilitate pathogen transmission and increase virulence. Therefore, species that live in social groups are predicted to suffer a higher pathogen burden, to invest more heavily in immune defence against pathogens, or both. However, there are few empirical tests of whether social species indeed invest more heavily in immune defence than non-social species. In the current study, we conducted a phylogenetically controlled comparison of innate immune response in Lamprologine cichlid fishes. We focused on three species of highly social cichlids that live in permanent groups and exhibit cooperative breeding (Julidochromis ornatus, Neolamprologus pulcher and Neolamprologus savoryi) and three species of non-social cichlids that exhibit neither grouping nor cooperative behaviour (Telmatochromis temporalis, Neolamprologus tetracanthus and Neolamprologus modestus). We quantified the innate immune response by injecting wild fishes with phytohaemagglutinin (PHA), a lectin that causes a cell-mediated immune response. We predicted that the three highly social species would show a greater immune reaction to the PHA treatment, indicating higher investment in immune defence against parasites relative to the three non-social species. We found significant species-level variation in immune response, but contrary to our prediction, this variation did not correspond to social system. However, we found that immune response was correlated with territory size across the six species. Our results indicate that the common assumption of a positive relationship between social system and investment in immune function may be overly simplistic. We suggest that factors such as rates of both in-group and out-group social interactions are likely to be important mediators of the relationship between sociality and immune function.

Hamilton Lab

Host diapause status and host diets augmented with cryoprotectants enhance cold hardiness in the parasitoid Nasonia vitripennis
Yuyan Li, Lisheng Zhang, Qirui Zhang, Hongyin Chen, David L. Denlinger. Journal of Insect Physiology. DOI: 10.1016/j.jinsphys.2014.08.005


Boosting cold hardiness in parasitoids is a goal that is particularly attractive for increasing shelf life and shipment of biological control agents. In the experiments reported here we use the parasitoid Nasonia vitripennis as a model to evaluate manipulations that may be capable of enhancing the wasp’s cold tolerance. We altered the parasitoid’s cold tolerance by manipulating the wasp’s diapause status, the diapause status of the host fly (Sarcophaga crassipalpis), and the diet of the host. Larval diapause in N. vitripennis dramatically increased cold tolerance and the diapause status of the host also exerted a positive, although less dramatic, effect. Augmenting the host fly’s diet with supplements of putative cryoprotectants (alanine, proline and glycerol) enhanced cold tolerance in parasitoids that fed on the flies, thus indicating a tri-trophic effect on parasitoid cold tolerance. The most pronounced improvement in cold tolerance was noted in parasitoids fed on fly hosts that had received a diet augmented with proline. These results suggest mechanisms that could be exploited for enhancement of cold tolerance in parasitoids of commercial interest.

Denlinger Lab

Development of 31 new microsatellite loci for two mole salamanders (Ambystoma laterale and A. jeffersonianum)
Robert D. Denton, H. Lisle Gibbs, Travis C. Glenn. Conservation Genetics Resources. August 2014


Ambystoma salamanders are amphibians that due to limited dispersal abilities and reliance on wetlands for breeding are susceptible to population declines and local extinctions (Blaustein et al. 2011). Species identification within Ambystoma is especially difficult due to the presence of unisexual Ambystoma that consist of multiple all-female lineages in which clones can have between two and five nuclear genomes from up to five other Ambystoma species (Bogart et al. 2007). The majority of these unisexual Ambystoma are composed of nuclear genomes from two species, A. laterale (Blue Spotted Salamander) and A. jeffersonianum (Jefferson Salamander). We developed species-specific microsatellite markers for these two species as a tool for the identification and investigation of the genetic interactions between sexual and unisexual groups in areas where either sexual species is endangered or of special conservation concern (Ohio, Indiana, and Ontario).

Gibbs Lab

Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms

Craig F. Barrett, John V. Freudenstein, Jeff Li, Dustin R. Mayfield-Jones, Leticia Perez, J. Chris Pires, Cristian Santos. Molecular Biology and Evolution.


Parasitic organisms exemplify morphological and genomic reduction. Some heterotrophic, parasitic plants harbor drastically reduced and degraded plastid genomes resulting from relaxed selective pressure on photosynthetic function. However, few studies have addressed the initial stages of plastome degradation in groups containing both photosynthetic and non-photosynthetic species. Corallorhiza is a genus of leafless, heterotrophic orchids that contains both green, photosynthetic species and non-green, putatively non-photosynthetic species, and represents an ideal system in which to assess the beginning of the transition to a ‘minimal plastome.’ Complete plastomes were generated for nine taxa of Corallorhiza using Illumina paired-end sequencing of genomic DNA to assess the degree of degradation among taxa, and for comparison with a general model of degradation among angiosperms. Quantification of total chlorophyll suggests that non-green Corallorhiza still produce chlorophyll, but at tenfold lower concentrations than green congeners. Complete plastomes and partial nuclear rDNA cistrons yielded a fully resolved tree for Corallorhiza, with at least two independent losses of photosynthesis, evidenced by gene deletions and pseudogenes in C. striata and non-green C. maculata. All Corallorhiza show some evidence of degradation in genes of the the NAD(P)H Dehydrogenase complex. Among genes with open reading frames, photosynthesis-related genes displayed evidence of neutral evolution in non-green Corallorhiza, while genes of the ATP Synthase complex displayed some evidence of positive selection in these same groups, though for reasons unknown. Corallorhiza spans the early stages of a general model of plastome degradation, and has added critical insight for understanding the process of plastome evolution in heterotrophic angiosperms.

Freudenstein Lab

A review of the subfamily Harpypalpinae Fain, 1972 (Acariformes: Harpirhynchidae)—parasites of passerine birds.  
Bochkov, Andre V. & Klompen, H. Zootaxa 3857(4): 451-477. DOI:

The subfamily Harpypalpinae Fain, 1972 (Acariformes: Cheyletoidea: Harpirhynchidae) is revised. Diagnoses of the subfamily and its two constituent genera, Harpypalpus Dubinin, 1957 and Harpypalpoides Lombert and Moss, 1979, and keys to females of all known species are provided. Data on harpypalpine hosts and distribution are summarized, and nine new species are described: Harpypalpus lonchura sp. nov. from Lonchura castaneothorax (Gould) (Estrildidae) in Australia, Harpypalpus pyrrhula sp. nov. from Pyrrhula pyrrhula (Linnaeus) (Fringillidae) in the Netherlands, Harpypalpus sturnus sp. nov. from Sturnus vulgaris Linnaeus (Sturnidae) in the Netherlands, Harpypalpus taeniopygia sp. nov. from Taeniopygia guttata (Vieillot) (Estrildidae) in Australia, Harpypalpoides hirundinoides sp. nov. from Hirundo rustica Linnaeus (Hirundinidae) in the Netherlands, Harpypalpoides johnstoni sp. nov. from Fringilla coelebs Linnaeus (Fringillidae) (type host) in the Netherlands and Fringilla montifringilla Linnaeus in Kazakhstan, Harpypalpoides regulus sp. nov. from Regulus regulus (Linnaeus) (Regulidae) in the Netherlands, Harpypalpoides sitta sp. nov. from Sitta pygmaea Vigors (Sittidae) in the USA (Arizona, California), and Harpypalpoides sylvia sp. nov. from Sylvia atricapilla (Linnaeus) (Sylviidae) in the Netherlands.

OSU Acarology