Publications by EEOB faculty December 1 - December 31

January 28, 2017
eeob 2016

Experimental whole-stream warming alters community size structure.

Nelson, D., Benstead, J. P., Huryn, A. D., Cross, W. F., Hood, J. M., Johnson, P. W., Junker, J. R., Gíslason, G. M. and Ólafsson, J. S. 2016. Glob Change Biol. doi:10.1111/gcb.13574


How ecological communities respond to predicted increases in temperature will determine the extent to which Earth's biodiversity and ecosystem functioning can be maintained into a warmer future. Warming is predicted to alter the structure of natural communities, but robust tests of such predictions require appropriate large-scale manipulations of intact, natural habitat that is open to dispersal processes via exchange with regional species pools. Here, we report results of a two-year whole-stream warming experiment that shifted invertebrate assemblage structure via unanticipated mechanisms, while still conforming to community-level metabolic theory. While warming by 3.8 °C decreased invertebrate abundance in the experimental stream by 60% relative to a reference stream, total invertebrate biomass was unchanged. Associated shifts in invertebrate assemblage structure were driven by the arrival of new taxa and a higher proportion of large, warm-adapted species (i.e., snails and predatory dipterans) relative to small-bodied, cold-adapted taxa (e.g., chironomids and oligochaetes). Experimental warming consequently shifted assemblage size spectra in ways that were unexpected, but consistent with thermal optima of taxa in the regional species pool. Higher temperatures increased community-level energy demand, which was presumably satisfied by higher primary production after warming. Our experiment demonstrates how warming reassembles communities within the constraints of energy supply via regional exchange of species that differ in thermal physiological traits. Similar responses will likely mediate impacts of anthropogenic warming on biodiversity and ecosystem function across all ecological communities.

Specialist and generalist symbionts show counterintuitive levels of genetic diversity and discordant demographic histories along the Florida Reef Tract.

Titus, B.M. & Daly, M. Coral Reefs. 2016. doi:10.1007/s00338-016-1515-z


Specialist and generalist life histories are expected to result in contrasting levels of genetic diversity at the population level, and symbioses are expected to lead to patterns that reflect a shared biogeographic history and co-diversification. We test these assumptions using mtDNA sequencing and a comparative phylogeographic approach for six co-occurring crustacean species that are symbiotic with sea anemones on western Atlantic coral reefs, yet vary in their host specificities: four are host specialists and two are host generalists. We first conducted species discovery analyses to delimit cryptic lineages, followed by classic population genetic diversity analyses for each delimited taxon, and then reconstructed the demographic history for each taxon using traditional summary statistics, Bayesian skyline plots, and approximate Bayesian computation to test for signatures of recent and concerted population expansion. The genetic diversity values recovered here contravene the expectations of the specialist–generalist variation hypothesis and classic population genetics theory; all specialist lineages had greater genetic diversity than generalists. Demography suggests recent population expansions in all taxa, although Bayesian skyline plots and approximate Bayesian computation suggest the timing and magnitude of these events were idiosyncratic. These results do not meet the a priori expectation of concordance among symbiotic taxa and suggest that intrinsic aspects of species biology may contribute more to phylogeographic history than extrinsic forces that shape whole communities. The recovery of two cryptic specialist lineages adds an additional layer of biodiversity to this symbiosis and contributes to an emerging pattern of cryptic speciation in the specialist taxa. Our results underscore the differences in the evolutionary processes acting on marine systems from the terrestrial processes that often drive theory. Finally, we continue to highlight the Florida Reef Tract as an important biodiversity hotspot.

Crowd control: sex ratio affects sexually selected cuticular hydrocarbons in male Drosophila serrata. 

Gershman, S. N. and Rundle, H. D. 2017. J. Evol. Biol. doi:10.1111/jeb.13028


Although it is advantageous for males to express costly sexually selected signals when females are present, they may also benefit from suppressing these signals to avoid costly interactions with rival males. Cuticular chemical profiles frequently function as insect sexual signals; however, few studies have asked whether males alter these signals in response to their social environment. In Drosophila serrata, an Australian fly, there is sexual selection for a multivariate combination of male cuticular hydrocarbons (CHCs). Here, we show that the ratio of females to males that an adult male experiences has a strong effect on his CHC expression, with female-biased adult sex ratios eliciting greater expression of CHC profiles associated with higher male mating success. Classical models predict that male reproductive investment should be highest when there is a small but nonzero number of rivals, but we found that males expressed the most attractive combination of CHCs when there were no rivals. We found that male CHCs were highly sensitive to adult sex ratio, with males expressing higher values of CHC profiles associated with greater mating success as the ratio of females to males increased. Moreover, sex ratio has a stronger effect on male CHC expression than adult density. Finally, we explore whether sex ratio affects the variance among a group of males in their CHC expression, as might be expected if individuals respond differently to a given social environment, but find little effect. Our results reveal that subtle differences in social environment can induce plasticity in male chemical signal expression.

Locomotor endurance predicts differences in realized dispersal between sympatric sexual and unisexual salamanders.

Denton, R. D., Greenwald, K. R. and Gibbs, H. L. 2016. Funct Ecol. doi:10.1111/1365-2435.12813


Dispersal is the central mechanism that determines connectivity between populations yet few studies connect the mechanisms of movement with realized dispersal in natural populations. To make such a link, we assessed how physiological variation among individuals predicted dispersal in natural populations of unisexual (all-female) and sexual Ambystoma salamanders on the same fragmented landscape in Ohio.
Specifically, we assessed variation in a trait that influences long-distance animal movement (locomotor endurance) and determined whether variation in endurance matched patterns of realized dispersal assessed using genetic assignment tests. A possible mechanism for why unisexuals would have lower locomotor endurance than a sympatric sexual species (Ambystoma texanum) is the potential energetic cost of evolutionarily mismatched mitochondrial and nuclear genomes within polyploid unisexuals.
We found that sexuals walked four times farther than unisexuals during treadmill endurance trials that mimic the locomotor endurance required for dispersal.
We then applied landscape genetic methods to identify dispersed adults and quantify realized dispersal. We show that the differences in locomotor endurance between unisexual and sexual salamanders scale to realized dispersal: dispersing sexual individuals travelled approximately twice the distance between presumed natal wetlands and the site of capture compared to dispersing unisexuals.
This study links variation in individual performance in terms of endurance with realized dispersal in the field and suggests a potential mechanism (physiological limitation due to mitonuclear mismatch) for the reduced endurance of unisexual individuals relative to sexual individuals although we discuss other possible explanations.
The differences in dispersal between these two types of salamanders also informs our understanding of sexual/unisexual coexistence by suggesting that unisexuals are at a competitive disadvantage in terms of colonization ability under a extinction-colonization model of coexistence.

Species Delimitation with Gene Flow

Nathan D. Jackson, Bryan C. Carstens, Ariadna E. Morales, Brian C. O'Meara. 2016.  Syst Biol. syw117. doi: 10.1093/sysbio/syw117


Species are commonly thought to be evolutionarily independent in a way that populations within a species are not. In recent years, studies that seek to identify evolutionarily independent lineages (i.e., to delimit species) using genetic data have typically adopted multispecies coalescent approaches that assume that evolutionary independence is formed by the differential sorting of ancestral alleles due to genetic drift. However, gene flow appears to be common among populations and nascent species, and while this process may inhibit lineage divergence (and thus independence), it is usually not explicitly considered when delimiting species. In this paper, we apply PHRAPL, a recently described method for phylogeographic model selection, to species delimitation. We describe an approach to delimiting species using PHRAPL that attempts to account for both genetic drift and gene flow, and we compare the method’s performance to that of a popular delimitation approach (BPP) using both simulated and empirical datasets. PHRAPL generally infers the correct demographic-delimitation model when the generating model includes gene flow between taxa, given a sufficient amount of data. When the generating model includes only isolation in the recent past, PHRAPL will in some cases fail to differentiate between gene flow and divergence, leading to model misspecification. Nevertheless, the explicit consideration of gene flow by PHRAPL is an important complement to existing delimitation approaches, particularly in systems where gene flow is likely important. [approximate likelihoods; coalescent simulations; genealogical divergence index; Homo sapiens; isolation-with-migration; multispecies coalescent; Sarracenia; Scincella]

Evolution of the Cytolytic Pore-Forming Proteins (Actinoporins) in Sea Anemones

Jason Macrander  and Marymegan Daly. 2016. Toxins 2016, 8(12), 368; doi:10.3390/toxins8120368


Sea anemones (Cnidaria, Anthozoa, and Actiniaria) use toxic peptides to incapacitate and immobilize prey and to deter potential predators. Their toxin arsenal is complex, targeting a variety of functionally important protein complexes and macromolecules involved in cellular homeostasis. Among these, actinoporins are one of the better characterized toxins; these venom proteins form a pore in cellular membranes containing sphingomyelin. We used a combined bioinformatic and phylogenetic approach to investigate how actinoporins have evolved across three superfamilies of sea anemones (Actinioidea, Metridioidea, and Actinostoloidea). Our analysis identified 90 candidate actinoporins across 20 species. We also found clusters of six actinoporin-like genes in five species of sea anemone (Nematostella vectensis, Stomphia coccinea, Epiactis japonica, Heteractis crispa, and Diadumene leucolena); these actinoporin-like sequences resembled actinoporins but have a higher sequence similarity with toxins from fungi, cone snails, and Hydra. Comparative analysis of the candidate actinoporins highlighted variable and conserved regions within actinoporins that may pertain to functional variation. Although multiple residues are involved in initiating sphingomyelin recognition and membrane binding, there is a high rate of replacement for a specific tryptophan with leucine (W112L) and other hydrophobic residues. Residues thought to be involved with oligomerization were variable, while those forming the phosphocholine (POC) binding site and the N-terminal region involved with cell membrane penetration were highly conserved.


Andria STAMMEN, Deb LAN,  Anita SCHUCHARDT, Kathy MALONE, Lin DING, Zakee SABREE. 2016. Education Research Highlights in Mathematics, Science and Technology.
This project aims to develop a measurement tool for assessing the conceptual understanding of secondary grade-level biology students (ages 11 to 18) that is reliable and valid. The study reported here describes the validity assessment of Secondary Biology Concept Inventory (S-BCI). A pool of assessment tasks was designed to target major biology constructs. The assessment items’ answer stems were developed to include distractors representing students’ alternative conceptions obtained from literature and student interviews. The validation stage of the S-BCI development involved an iterative revision and review process to help establish sufficient S-BCI content and construct validity. This stage included (i) student interviews and (ii) multi-expert panel critique. Based on the results of the aforementioned analyses, assessment items were proven to be validwhere included on the S-BCI.

Improved Feedstock Option or Invasive Risk? Comparing Establishment and Productivity of Fertile Miscanthus × giganteus to Miscanthus sinensis

Bonin, C.L., Mutegi, E., Snow, A.A. et al. Bioenerg. Res. 2016. doi:10.1007/s12155-016-9808-1


The perennial grass genus Miscanthus has great promise as biomass feedstock, but there are concerns about potential invasion outside production fields. While the sterile hybrid Miscanthus × giganteus is currently one of the leading feedstock options due to its low invasive potential, fertile varieties are being developed to reduce establishment costs, and their invasive risks need to be further assessed. We performed seed addition experiments in Ohio and Iowa, USA to examine the establishment, flowering, persistence, and shoot biomass per plot of a fertile M. × giganteus biotype (‘PowerCane’) and two Miscanthus sinensis biotypes, one feral, and one ornamental. Seeds were added to small, replicated plots in each of the 2 years under two seeding densities and two competition treatments, and plots were monitored for 2–3 years. The ‘PowerCane’ biotype established better, survived better, and produced greater amounts of biomass per plot than both M. sinensis biotypes. All three biotypes flowered by the second or third year after establishment, with inflorescences more numerous in ‘PowerCane’ and the Ornamental M. sinensis biotypes. Effects of seeding density and competition on these patterns were minor in most cases. Our research suggests that ‘PowerCane’ exhibits many traits shared by both biomass crops and invasive species: multi-year persistence, high biomass potential, and fertility. We suggest that the benefits of a seeded M. × giganteus should be carefully weighed against its increased invasive risk prior to deployment across the landscape.

Statistical hybrid detection and the inference of ancestral distribution areas in Tolpis (Asteraceae).



Many historical biogeographic studies do not account for the effect of hybrid taxa on phylogenetic tree inference, despite recent advances in the statistical identification of such taxa. This investigation aims to illustrate the impact that hybrid taxa can have on ancestral area reconstructions of the plant genus Tolpis, which displays an evolutionary history possibly indicative of a back-colonization of the continental Mediterranean. We evaluate and apply two statistical hybrid detection methods, JML and STEM-hy, which assist in identifying reticulate patterns of allele coalescence. We also evaluate and apply a software tool, P2C2M, to test the fit of genetic loci to the multispecies coalescent model (MSCM). The application of these tools to a previously published data set of three nuclear DNA markers indicates the presence of several potential hybrid taxa in Tolpis. One nuclear marker is found to display a reduced level of reticulate history, a good fit to the MSCM and minimal signal of gene flow across archipelagoes. Ancestral distribution areas are reconstructed on gene and species trees of Tolpis before and after the exclusion of putative hybrid taxa using stochastic character mapping, parameterized likelihood reconstructions, and reconstructions under continuous-time Markov chain models. The results of these reconstructions indicate that taxa of hybrid origin may have a considerable impact on ancestral area reconstruction and that it is important to account for such taxa prior to biogeographic analysis. We conclude that Tolpis has likely had a time-consistent distribution in island habitats and originated on the Canary Islands.