Ohio State nav bar

EEOB Publications April 1 - April 30

April 24, 2021

EEOB Publications April 1 - April 30

EEOB department silhouette graphic in black & white

Multiple concurrent and convergent stages of genome reduction in bacterial symbionts across a stink bug family

Alejandro Otero-Bravo & Zakee L. Sabree. 2021. Scientific Reports volume 11, Article number: 7731. https://doi.org/10.1038/s41598-021-86574-8

Abstract

Nutritional symbioses between bacteria and insects are prevalent and diverse, allowing insects to expand their feeding strategies and niches. A common consequence of long-term associations is a considerable reduction in symbiont genome size likely influenced by the radical shift in selective pressures as a result of the less variable environment within the host. While several of these cases can be found across distinct insect species, most examples provide a limited view of a single or few stages of the process of genome reduction. Stink bugs (Pentatomidae) contain inherited gamma-proteobacterial symbionts in a modified organ in their midgut and are an example of a long-term nutritional symbiosis, but multiple cases of new symbiont acquisition throughout the history of the family have been described. We sequenced the genomes of 11 symbionts of stink bugs with sizes that ranged from equal to those of their free-living relatives to less than 20%. Comparative genomics of these and previously sequenced symbionts revealed initial stages of genome reduction including an initial pseudogenization before genome reduction, followed by multiple stages of progressive degeneration of existing metabolic pathways likely to impact host interactions such as cell wall component biosynthesis. Amino acid biosynthesis pathways were retained in a similar manner as in other nutritional symbionts. Stink bug symbionts display convergent genome reduction events showing progressive changes from a free-living bacterium to a host-dependent symbiont. This system can therefore be used to study convergent genome evolution of symbiosis at a scale not previously available.


Synergism between local‐ and landscape‐level pesticides reduces wild bee floral visitation in pollinator‐dependent crops

Elias H. Bloom  Thomas J. Wood  Keng‐Lou James Hung  John J. Ternest  Laura L. Ingwell  Karen Goodell  Ian Kaplan  Zsofia Szendrei. 2021. https://doi.org/10.1111/1365-2664.13871

Abstract

The hazard pesticides pose to pollinators are well‐understood from laboratory studies. However, the field‐level response of pollinators to pesticide use in agroecosystems is not well‐established, nor is it clear if synergisms between pesticides affect pollinator visitation to crops.
Here, we evaluated if fungicide and insecticide use posed a hazard to wild and honeybees at 87 cucurbit—pumpkin, cucumber, watermelon—farms in the Midwestern United States. We also evaluated if synergisms between local‐ (i.e. focal cucurbit field) and landscape‐level (i.e. surrounding crops) pesticide use influence wild and honeybee visitation to crop flowers.
We found that bees were exposed to pesticides above regulatory levels of concern and that synergisms between a few local insecticides and landscape‐level fungicides reduced wild bee visitation to cucurbit flowers. Honey and bumblebee visitation to crops was not strongly influenced by synergisms between pesticides used at the local and landscape level.
Synthesis and applications. We found pesticides posed hazards to honey and wild bee species. However, pesticides were less likely to affect short‐term visitation rates of honeybees compared with wild bee species. Thus, there is a need for changes in pesticide use at large spatial scales to reduce reliance on honeybees and maximize wild bee visitation to pollinator‐dependent crops. We suggest that a multifaceted approach, involving collaborations between farmers, consumers and policymakers, will be fruitful to promote changes in pesticide use and wild bee pollinators.


Determinants of invertebrate community structure in glacial‐melt streams of southeast Tibet

Heather Fair  Peter C. Smiley Jr  Roman Lanno. 2021. https://doi.org/10.1111/fwb.13716

Abstract

A widely examined predictive model of invertebrate community dynamics in glacial‐melt streams describes longitudinal changes in community structure with changing water temperature and channel stability with increasing distance from glaciers. Previous studies conducted in Europe, Greenland, New Zealand, and South America have supported the predictions of the invertebrate model and contributed to its refinement. However, none has evaluated if the model fits invertebrate community dynamics over a full range of distances from the glacier and water temperature conditions within glacial‐melt streams in southeast Tibet.
We sampled invertebrates and measured water temperature, specific conductivity, turbidity, and associated glacier‐related variables within 14 sites in three subalpine glacial‐melt catchments in southeastern Tibet's Three Parallel Rivers region during 2010, 2011, 2013, and 2015. Our sites encompassed a temperature gradient from the upstream metakryal sites (maximum summer water temperature <2°C) to the furthest downstream site (maximum summer temperature >10°C) near the Mekong River.
We evaluated the relationships of invertebrate community structure with in situ water temperature and channel stability which are the focal habitat variables in the invertebrate model. The additional habitat variables of distance from the glacier, glacier size, conductivity, and turbidity were evaluated to see if these were more important determinants of community structure than in situ water temperature and channel stability.
Minimum and in situ water temperatures were positively correlated with distance from the glacier but Pfankuch Channel Stability Index bottom scores were not. Thus, the physical template within our study area differed from the expected template of the invertebrate model.
Similar to the invertebrate model, in situ water temperature by itself or combined with Pfankuch index best explained five invertebrate response variables. In contrast with the invertebrate model, conductivity and turbidity best explained invertebrate taxa richness, density, and the site scores of the first and second detrended correspondence analysis axes of relative abundance.
The invertebrate model predicts that only Diamesinae will occur in metakryal sites. However, in our metakryal sites we frequently captured 13 taxa (two Nemouridae morphotypes, Diamesinae, Orthocladiinae, Rhyacophila, Epeorus, Taeniopterygidae, Baetis, Capnia, Simuliidae, Limnephilidae, Himalopsyche, and Collembola).
Invertebrate‐habitat relationships and taxa occurrence trends in glacial‐melt catchments in southeast Tibet differed from the invertebrate model predictions. Our findings highlight the need to develop a regional version of the invertebrate model applicable to Asian glacial‐melt streams with unstable stream channels throughout their catchments and that do not freeze in the winter.


Predicting migration routes for three species of migratory bats using species distribution models

Jamin G. Wieringa​, Bryan C. Carstens, H Lisle Gibbs. 2021. PeerJ 9:e11177 https://doi.org/10.7717/peerj.11177

Abstract

Understanding seasonal variation in the distribution and movement patterns of migratory species is essential to monitoring and conservation efforts. While there are many species of migratory bats in North America, little is known about their seasonal movements. In terms of conservation, this is important because the bat fatalities from wind energy turbines are significant and may fluctuate seasonally. Here we describe seasonally resolved distributions for the three species that are most impacted by wind farms (Lasiurus borealis (eastern red bat), L. cinereus (hoary bat) and Lasionycteris noctivagans (silver-haired bat)) and use these distributions to infer their most likely migratory pathways. To accomplish this, we collected 2,880 occurrence points from the Global Biodiversity Information Facility over five decades in North America to model species distributions on a seasonal basis and used an ensemble approach for modeling distributions. This dataset included 1,129 data points for L. borealis, 917 for L. cinereus and 834 for L. noctivagans. The results suggest that all three species exhibit variation in distributions from north to south depending on season, with each species showing potential migratory pathways during the fall migration that follow linear features. Finally, we describe proposed migratory pathways for these three species that can be used to identify stop-over sites, assess small-scale migration and highlight areas that should be prioritized for actions to reduce the effects of wind farm mortality.


Solvent choice influences final toxicity results in Thamnocephalus platyurus bioassay when exposed to microcystin -LR

Carissa Hipsher, Joel Barker, Roman Lanno, Allison MacKay. 2021. https://doi.org/10.1016/j.toxicon.2021.04.010

Abstract

Cyanobacterial blooms present a threat to many waterbodies around the world used for drinking water and recreational purposes. Toxicology tests, such as the Thamnotoxkit-F which uses the cladoceran T. platyurus, have been employed to assess the health hazards that these blooms may pose to the public. However, reported median lethal concentrations (LC50) of microcystin -LR to T. platyurus vary significantly from one study to the next. The variation in solvent type and concentrations used to dissolve microcystin -LR in preparation for toxicity experiments may be contributing to the variations in LC50 values found in the literature. The primary goal of this study was to determine what solvents and their corresponding concentrations can be used for microcystin -LR testing using T. platyurus without artifactually impacting LC50 values. All toxicity testing was completed using glassware as polystyrene containers have been shown to sorb microcystin. Microcystin -LR LC50 values for T. platyurus were determined using United States Environmental Protection Agency (US EPA) moderately hard standard freshwater as a control for comparison with systems that were prepared using dimethyl sulfoxide or methanol to dissolve microcystin -LR. Low levels of dimethyl sulfoxide (2%) or methanol (1%) did not impact LC50 values of microcystin -LR to T. platyurus compared to US EPA moderately hard standard freshwater diluted in microcystin -LR. However, higher levels of dimethyl sulfoxide (4%) and methanol (1.4% and 4%) did lower the LC50 for microcystin -LR to T. platyurus, consistent with the toxicity of these solvents to T. platyurus when dosed in the absence of microcystin -LR. Researchers need to report the type and concentrations of solvents used in toxicity tests using cyanotoxins in order to ensure that results can be intercompared appropriately. Furthermore, researchers need to use caution when using organic solvents such as dimethyl sulfoxide or methanol to ensure that these solvents are not causing significant mortality in toxicity testing.


Influence of Stocking Practices, Predation, and Reservoir Characteristics on the Growth and Recruitment of Saugeye

Richard R. Budnik, Jahn L. Kallis, Elizabeth A. Marschall. 2021. North American Journal of Fisheries Management. https://doi.org/10.1002/nafm.10624

Abstract

Saugeye (female Sander vitreus X male S. canadensis) are stocked annually into Ohio reservoirs to maintain popular recreational fisheries. The growth and recruitment of stocked saugeye are highly variable among years and reservoirs, with the causes of this variability not well understood. Using a multi‐year (2004‐2019), multi‐reservoir (6 reservoirs) dataset, we implemented mixed‐effects models and an information theoretic approach to identify possible predictors of saugeye post‐stocking growth and recruitment. Top‐performing models (ΔAICc < 2) explained 38‐40% of the variation in stocked saugeye growth (N = 4 models) and 36‐47% of the variation in stocked saugeye recruitment (N = 9 models). Specifically, our growth models identified stocking day of year and mean summer (July‐August) water temperature as significant predictors, with saugeye experiencing higher daily growth rates when fish were stocked earlier in the year and when summer water temperatures were warmer. Based on the results from our recruitment models, stocking density was identified as the only significant predictor, with greater stocking densities leading to stronger stocked saugeye recruitment. From these relationships, we predict that saugeye fishery production will be greater when managers stock greater densities of saugeye earlier in the year and when summer reservoir temperatures are higher. Despite identifying significant predictors, our models could not explain much of the variation in stocked saugeye growth and recruitment, revealing the complexity of growth and recruitment processes in Ohio reservoirs.


Phylogenetically diverse diets favor more complex venoms in North American pitvipers

Holding, Matthew L. ; Strickland, Jason L. ; Rautsaw, Rhett M. ; Hofmann, Erich P. ; Mason, Andrew J. ; Hogan, Michael P. ; Nystrom, Gunnar S. ; Ellsworth, Schyler A. ; Colston, Timothy J. ; Borja, Miguel ; Castañeda-Gaytán, Gamaliel ; Grünwald, Christoph I. ; Jones, Jason M. ; Freitas-de-Sousa, Luciana A. ; Viala, Vincent Louis ; Margres, Mark J. ; Hingst-Zaher, Erika ; Junqueira-de-Azevedo, Inácio L. M. ; Moura-da-Silva, Ana M. ; Grazziotin, Felipe G. ; Gibbs, H. Lisle ; Rokyta, Darin R. ; Parkinson, Christopher L. PNAS April 27, 2021 118 (17) e2015579118; https://doi.org/10.1073/pnas.2015579118

Abstract

The role of natural selection in the evolution of trait complexity can be characterized by testing hypothesized links between complex forms and their functions across species. Predatory venoms are composed of multiple proteins that collectively function to incapacitate prey. Venom complexity fluctuates over evolutionary timescales, with apparent increases and decreases in complexity, and yet the causes of this variation are unclear. We tested alternative hypotheses linking venom complexity and ecological sources of selection from diet in the largest clade of front-fanged venomous snakes in North America: the rattlesnakes, copperheads, cantils, and cottonmouths. We generated independent transcriptomic and proteomic measures of venom complexity and collated several natural history studies to quantify dietary variation. We then constructed genome-scale phylogenies for these snakes for comparative analyses. Strikingly, prey phylogenetic diversity was more strongly correlated to venom complexity than was overall prey species diversity, specifically implicating prey species’ divergence, rather than the number of lineages alone, in the evolution of complexity. Prey phylogenetic diversity further predicted transcriptomic complexity of three of the four largest gene families in viper venom, showing that complexity evolution is a concerted response among many independent gene families. We suggest that the phylogenetic diversity of prey measures functionally relevant divergence in the targets of venom, a claim supported by sequence diversity in the coagulation cascade targets of venom. Our results support the general concept that the diversity of species in an ecological community is more important than their overall number in determining evolutionary patterns in predator trait complexity.


The Chemosensory Repertoire of the Eastern Diamondback Rattlesnake (Crotalus adamanteus) Reveals Complementary Genetics of Olfactory and Vomeronasal-Type Receptors

Michael P. Hogan, A. Carl Whittington, Michael B. Broe, Micaiah J. Ward, H. Lisle Gibbs & Darin R. Rokyta. J Mol Evol 89, 313–328 (2021). https://doi.org/10.1007/s00239-021-10007-3

Abstract

Pitviper sensory perception incorporates diverse stimuli through the integration of trichromatic color vision, bifocal heat-sensing, and dual-system chemoperception. Chemoperception, or olfaction, is mediated by chemoreceptors in the olfactory bulb and the vomeronasal organ, but the true genomic complexity of the gene families and their relative contributions is unknown. A full genomic accounting of pitviper chemoperception directly complements our current understanding of their venoms by generating a more complete polyphenic representation of their predatory arsenal. To characterize the genetic repertoire of pitviper chemoperception, we analyzed a full-genome assembly for Crotalus adamanteus, the eastern diamondback rattlesnake. We identified hundreds of genes encoding both olfactory receptors (ORs; 362 full-length genes) and type-2 vomeronasal receptors (V2Rs; 430 full-length genes). Many chemoreceptor genes are organized into large tandem repeat arrays. Comparative analysis of V2R orthologs across squamates demonstrates how gene array expansion and contraction underlies the evolution of the chemoreceptor repertoire, which likely reflects shifts in life history traits. Chromosomal assignments of chemosensory genes identified sex chromosome specific chemoreceptor genes, providing gene candidates underlying observed sex-specific chemosensory-based behaviors. We detected widespread episodic evolution in the extracellular, ligand-binding domains of both ORs and V2Rs, suggesting the diversification of chemoreceptors is driven by transient periods of positive selection. We provide a robust genetic framework for studying pitviper chemosensory ecology and evolution.


Ecosystem change as a driver of fish recruitment dynamics: A case study of two Lake Erie yellow perch populations

Benjamin J. Marcek, Troy M. Farmer, Elizabeth A. Marschall, Giovanni Petris, Stuart A. Ludsin. 2021. https://doi.org/10.1111/fwb.13707

Abstract

Although previous research has identified ways in which environmental conditions influence population processes in many ecosystems, these relationships often weaken or break down with the inclusion of additional years of data, for reasons that remain unclear.

To better understand if and how the relationships between historically important environmental drivers of yellow perch (Perca flavescens) recruitment varied during 1969–2018 in two Lake Erie basins characterised by contrasting productivity, we used dynamic linear modelling, which allows for nonstationary relationships between predictor and response variables to be quantified.

Our analyses revealed that abiotic conditions during egg and larval development (i.e. winter temperature, springtime river inflows, and thermal conditions) were important in the productive west basin, whereas a combination of abiotic (i.e. winter temperature and river inflows) and biotic (i.e. small-bodied and large-bodied predators) conditions were important in the less-productive central basin.

While the importance of most environmental factors to yellow perch recruitment remained static through time, the importance of river inflows changed through time in the west and central basins. Large-bodied predators (i.e. walleye, Sander vitreus) also varied in their importance through time in the central basin. These changes in recruitment drivers were independent of temporal changes to the environmental conditions themselves, coinciding instead with the timing of major shifts in Lake Erie's nutrient status.

Our results demonstrate that ecosystem change can cause the relationships between environmental conditions and population processes (e.g. recruitment) of aquatic organisms to vary through time and space. They also highlight the value of periodically revisiting their applicability, especially if these relationships are used to help manage or sustain populations in ecosystems experiencing human-driven environmental change.


Comparative phylogeography of two Northern Rocky Mountain endemics: the widespread Anguispira kochi occidentalis and the narrow-range Anguispira nimapuna (Gastropoda: Discidae)

Andrew M Rankin, Frank E Anderson, Stephanie A Clutts, Anahí Espíndola, Bryan C Carstens, Michael Lucid, Jack Sullivan. 2021. Biological Journal of the Linnean Society. blab030. https://doi.org/10.1093/biolinnean/blab030

Abstract

The Northern Rocky Mountain ecosystem supports rich biological diversity with many endemic and rare species. Extant endemics display two biogeographic patterns: widespread species with fragmented populations, and narrow-range endemics. These distributions are shown by the congeneric snails Anguispira kochi occidentalis and Anguispira nimapuna. These two taxa are disjunct from the remaining species of the genus, which achieves its greatest diversity in eastern North America. Given the disjunct nature of A. k. occidentalis and A. nimapuna, we here present a mtDNA phylogeny of the genus that includes both eastern and western species to assess the phylogenetic position of A. k. occidentalis and A. nimapuna. We then reconstruct the demographic history of A. k. occidentalis and A. nimapuna by analysing current patterns of genetic variation and interpreting the results considering the historical biogeography of the region. Both A. k. occidentalis and A. nimapuna represent unique taxa that are genetically and geographically distinct from their congeners. The current distribution and genetic structure of A. k. occidentalis has been shaped by both historical isolation in refugia and more recent northward shifts, whereas A. nimapuna is represented by two populations with shallow divergence in an area of long-term habitat stability.