Ohio State nav bar

Publications by EEOB faculty April 1 - April 30

April 25, 2016

Publications by EEOB faculty April 1 - April 30

EEOB graphic 2016

Multimodal Communication in Wolf Spiders (Lycosidae)—An Emerging Model for Study

G.W. Uetz, , D.L. Clark, J.A. Roberts. 2016. Advances in the Study of Behavior. doi:10.1016/bs.asb.2016.03.003

Abstract

The subject of communication in spiders is of growing interest to animal behaviorists and evolutionary biologists for many reasons. Communication is critical for spiders, as they are predatory and potentially cannibalistic and thus positioned uniquely at the intersection of sexual and natural selection. Spiders have a very different sensory world, or “umwelt” than better-studied taxa (such as vertebrates and insects) and perceive their world through substratum vibration (eg, environmental surfaces or the silk strands of webs), chemotactile or olfactory cues (eg, silk-borne or airborne pheromones), and widely varying visual capabilities (ranging from rudimentary light/dark perception to high-resolution visual acuity). Perhaps as a consequence, spiders exhibit a great diversity of communication behaviors. Spiders also have a relatively simple central nervous system (CNS), yet they can integrate sensory input from multiple sources and systems at the same time. Finally, like many invertebrates, spiders are small in size and often easy to work within the laboratory and/or field.

In a recent meta-analysis of the representation of various sensory modalities and taxa in sensory studies, Coleman (2009) suggested that invertebrates and particularly spiders are underrepresented:

Of the taxa that represent less than three percent of the studies…spiders seem particularly underrepresented given the widespread occurrence of elaborate courtship displays in several genera…Indeed, I suggest that it has been spiders that have yielded the greatest insight into the importance of multimodal communication in mate choice.


Despite this general underrepresentation, over the past several decades, research has examined spider signaling modes, female mate preferences, environmental constraints, and eavesdropping by conspecific males and predators using a variety of approaches in lab and field. Ever since the seminal work “Spider communication: mechanisms and ecological significance” edited by Witt and Rovner (1982), the literature of this field has grown exponentially (Fig. 1). There have been several excellent reviews since then (Eberhard, 1994, Elgar, 1998, Gaskett, 2007, Huber, 2005, Schulz, 2013 and Uhl and Elias, 2011). More recently, owing to advances in the technologies available to record, analyze, and experiment with these tiny invertebrates and their signals, and the diversity of behaviors exhibited by certain taxa, there has been a growing recognition of spiders as excellent models for investigating questions about communication and sexual selection (Herberstein and Hebets, 2013 and Herberstein et al., 2014). In the review that follows, we provide a survey of the history, depth, and breadth of research surrounding wolf spiders, highlighting our own work and the work of colleagues to provide justification for why the Lycosidae, and Schizocosa in particular are indispensable for our collective understanding of multimodal communication and mate choice.


No evidence for larger brains in cooperatively breeding cichlid fishes

 

Adam R. Reddon,*a Constance M. O’Connor,†a Isaac Y. Ligocki,b Jennifer K. Hellmann,b Susan E. Marsh-Rollo,a Ian M. Hamilton,bc Sigal Balshinea. 2016. Canadian Journal of Zoology, 10.1139/cjz-2015-0118.

Abstract

The social brain hypothesis posits that frequent social interactions, characteristic of group living species, select for greater socio-cognitive abilities and the requisite neural machinery. An extension of the social brains hypothesis, known as the cooperative breeding brain hypothesis, postulates that cooperatively breeding species, which live in stable social groups and provide allocare, face particularly pronounced cognitive demands because they must recognize, remember, and differentially respond to multiple group members. These socio-cognitive challenges are thought to have selected for increased cognitive capacity, supported by a bigger brain. To test the prediction that cooperative breeders have larger brains, we performed a phylogenetically controlled comparison of the whole brain masses of adult fish from 16 closely related species of cooperatively and independently breeding lamprologine cichlid species from Lake Tanganyika. We collected data on brain mass from males of eight species of lamprologine cichlids and added this to brain mass data from eight more species found in the published literature. Controlling for body size and phylogeny, we found that cooperative breeding species did not have larger brains, and this was true of for both our field-collected data set and the expanded data set including published values. This study adds to a growing body of literature from other taxa that cast doubt on the cooperative breeding brain hypothesis.


Mechanisms of Animal Diapause: Recent Developments from Nematodes, Crustaceans, Insects, and Fish

 

Steven C. Hand, David L. Denlinger, Jason E. Podrabsky, Richard Roy. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology Published 6 April 2016 Vol. no. , DOI: 10.1152/ajpregu.00250.2015.

Abstract

Life cycle delays are beneficial for opportunistic species encountering suboptimal environments. Many animals display a programmed arrest of development (diapause) at some stage(s) of their development, and the diapause state may or may not be associated with some degree of metabolic depression. In this review, we will evaluate current advancements in our understanding of the mechanisms responsible for the remarkable phenotype, as well as environmental cues that signal entry and termination of the state. The developmental stage at which diapause occurs dictates and constrains the mechanisms governing diapause. Considerable progress has been made in clarifying proximal mechanisms of metabolic arrest and the signaling pathways like insulin/Foxo that control gene expression patterns. Overlapping themes are also seen in mechanisms that control cell cycle arrest. Evidence is emerging for epigenetic contributions to diapause regulation via small RNAs in nematodes, crustaceans, insects, and fish. Knockdown of circadian clock genes in selected insect species supports the importance of clock genes in the photoperiodic response that cues diapause. A large suite of chaperone-like proteins, expressed during diapause, protects biological structures during long periods of energy-limited stasis. More information is needed to paint a complete picture of how environmental cues are coupled to the signal transduction that initiates the complex diapause phenotype, as well as molecular explanations for how the state is terminated. Excellent examples of molecular memory in post-dauer animals have been documented in Caenorhabditis elegans. It is clear that a single suite of mechanisms does not regulate diapause across all species and developmental stages.


Enhanced stress responses and metabolic adjustments linked to diapause and onset of migration in the large milkweed bug Oncopeltus fasciatus

 

Charles A. E. Dean, Nicholas M. Teets, Vladimir Koštál, Petr Šimek andDavid L. Denlinger. 2016. DOI: 10.1111/phen.12140.

Abstract

In response to short-day photoperiods in the autumn, the large milkweed bug Oncopeltus fasciatus Dallas enters a reproductive diapause and migrates south to avoid the adverse environmental conditions and food shortages that prevail in the winter. Milkweed bugs are one of only a few temperate insects that undergo long distance migration during diapause, making them a good model for investigating trade-offs associated with migratory diapause. Although enhanced stress tolerance is typical of diapause, it is unclear whether this aspect of diapause would be retained in a species that migrates to more favourable conditions. The present study tests (i) whether diapause enhances thermal tolerance; (ii) whether food shortage, which is required for maximal expression of diapause, influences thermal tolerance during diapause; and (iii) whether the potential changes in stress tolerance are associated with upregulated heat shock protein expression or metabolic adjustments (including cryoprotectant synthesis), or both. Both cold tolerance at −10 °C and heat tolerance at 43 °C are significantly higher in diapausing O. fasciatus, whereas food restriction has no further effect on thermal tolerance. None of the heat shock protein transcripts measured are significantly upregulated in response to diapause, and the experiments also fail to detect any cryoprotectant accumulation during diapause. Thus, although heat shock proteins and cryoprotectants are common mechanisms for enhancing thermal tolerance in many diapausing insects, the results of the present study suggest that alternative mechanisms are responsible in milkweed bugs.


Community trees: identifying codiversification in the páramo dipteran community

Bryan Carstens, Michael Gruenstaeudl and Noah Reid. 2016. DOI: 10.1111/evo.12916

Abstract

Groups of codistributed species that responded in a concerted manner to environmental events are expected to share patterns of evolutionary diversification. However, the identification of such groups has largely been based on qualitative, post hoc analyses. We develop here two methods (PPS, K-F ANOVA) for the analysis of codistributed species that, given a group of species with a shared pattern of diversification, allow empiricists to identify those taxa that do not codiversify (i.e., "outlier" species). The identification of outlier species makes it possible to jointly estimate the evolutionary history of co-diversifying taxa. To evaluate the approaches presented here, we collected data from Páramo dipterans, identified outlier species, and estimated a "community tree" from species that are identified as having co-diversified. Our results demonstrate that dipteran communities from different Páramo habitats in the same mountain range are more closely related than communities in other ranges. We also conduct simulation testing to evaluate this approach. Results suggest that our approach provides a useful addition to comparative phylogeographic methods, while identifying aspects of the analysis that require careful interpretation. In particular, both the PPS and K-F ANOVA perform acceptably when there are one or two outlier species, but less so as the number of outliers increase. This is likely a function of the corresponding degradation of the signal of community divergence; without a strong signal from a co-diversifying community, there is no dominant pattern from which to detect and outlier species. For this reason, both the magnitude of K-F distance distribution and outside knowledge about the phylogeographic history of each putative member of the community should be considered when interpreting results.


Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas

Ludmila Tyler, Scott J. Lee, Nelson D. Young, Gregory A. DeIulio, Elena Benavente, Michael Reagon, Jessica Sysopha, Riccardo M. Baldini, Angelo Troìa, Samuel P. Hazen, and Ana L. Caicedo. 2016.  doi:10.3835/plantgenome2015.08.0074

Abstract
The small, annual grass Brachypodium distachyon, a close relative of wheat and barley, 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 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 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 single-nucleotide polymorphisms 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. GWAS investigations 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. Studying inherited natural variation can elucidate the genetic basis of complex, multi- genic traits. In particular, next-generation genotyping has enabled genome-wide association studies (GWAS), which examine large, diverse populations for correlations between alleles at individual markers and phenotypes of interest. The GWAS approach has been successful in a number of plant species, including rice (Oryza sativa), maize (Zea mays), barley (Hordeum vulgare), the bioenergy grass Miscanthus, and the dicotyledenous model Arabidopsis thaliana (Atwell et al., 2010; Huang et al., 2010; Tian et al., 2011; Pasam et al., 2012; Slavov et al., 2014). With the increasing demand for plants as sources of food, feed, and fuel, there is a growing need for tools to improve our understanding of agronomically important traits. Whether the investigations are performed in crops or model species, the success of GWAS depends on the availability of extensive, diverse, and well-characterized germplasm collections.

 
Here, we expand the germplasm resources available for the model grass Brachypodium distachyon. Brachypodium distachyon was first proposed as a model research organism nearly 15 years ago (Draper et al., 2001) and has rapidly developed into a powerful system with a wealth of research tools (Brkljacic et al., 2011; Mur et al., 2011; Girin et al., 2014). As a small, diploid annual with a compact, sequenced genome (International Brachypodium Initiative, 2010) and amenability to both crossing and genetic transformation (Vain et al., 2008; Vogel and Hill, 2008; Alves et al., 2009; Bragg et al., 2012), B. distachyon has many of the advantages of the preeminent plant model, A. thaliana (Koornneef and Meinke, 2010). However, unlike A. thaliana, B. distachyon is in the Pooideae subfamily of the grasses, together with wheat (Triticum aestivum), oat (Avena sativa), and barley (Hordeum vulgare), and is thus an especially valuable model for the temperate cereals (Mochida and Shinozaki, 2013). Because it has the type II cell walls typical of grasses, B. distachyon is also being used to investigate feedstock properties for bioenergy production (Gomez et al., 2008; Lee et al., 2012; Marriott et al., 2014; Tyler et al., 2014). Despite all these advantages, germplasm collections of B. distachyon remain limited. Although the native range of B. distachyon stretches across the Mediterranean region (Garvin et al., 2008; López-Alvarez et al., 2015), material from only two countries, Spain and Turkey, has been characterized in detail. This limitation has hindered assessment of structure and other population parameters in the species, as well as development of a diverse germplasm collection for GWAS. Until recently, the diploid B. distachyon, with a haploid chromosome number of 5, was grouped in the same species with morphologically similar Brachypodium plants that have haploid chromosome numbers of 10 and 15. These latter two cytotypes are now considered separate species: B. stacei (n = 10) and B. hybridum (n = 15) (Catalán et al., 2012). Fluorescence and genomic in situ hybridization have elegantly demonstrated that B. hybridum is an allotetraploid arising from interbreeding between diploid, B. distachyon-like and B. stacei-like parents (Hasterok et al., 2004; Idziak et al., 2011; Catalán et al., 2012). Flow cytometry has shown that the genome of B. hybridum is approximately twice the size of the B. stacei or B. distachyon genome (Catalán et al., 2012). Furthermore, DNA barcoding and PCR-based analysis of simple sequence repeats (SSRs) have emerged as methods for Brachypodium species identification (Giraldo et al., 2012; López-Alvarez et al., 2012). While B. stacei and B. hybridum are useful for investigating speciation and ploidy, B. distachyon has remained the premier model system within this genus, and it is crucial to correctly distinguish the three species when developing germplasm resources for GWAS. In this study, we undertook the collection and characterization of 54 new Brachypodium accessions, together with 40 previously described lines, originating from the northern arc of the Mediterranean region and the Middle East. Our collection includes novel material from Spain, Italy, Albania, Georgia, and Armenia. We performed reduced-representation sequencing to generate a large collection of polymorphic markers, which allowed us to both differentiate between species and elucidate the population structure within B. distachyon. Interestingly, we identified flowering time as a major factor correlated with population structure. Despite this correlation, and the occurrence of strong structure in the species, we were able to use flowering time as an example to illustrate the feasibility of GWAS and limits to its resolution in our extended germplasm panel.

Model-based analysis supports interglacial refugia over long-dispersal events in the diversification of two South American cactus species

M F Perez1,3, I A S Bonatelli1,3, E M Moraes1 and B C Carstens. 2016. doi: 10.1038/hdy.2016.17Abstract
Pilosocereus machrisii and P. aurisetus are cactus species within the P. aurisetus complex, a group of eight cacti that are restricted to rocky habitats within the Neotropical savannas of eastern South America. Previous studies have suggested that diversification within this complex was driven by distributional fragmentation, isolation leading to allopatric differentiation, and secondary contact among divergent lineages. These events have been associated with Quaternary climatic cycles, leading to the hypothesis that the xerophytic vegetation patches which presently harbor these populations operate as refugia during the current interglacial. However, owing to limitations of the standard phylogeographic approaches used in these studies, this hypothesis was not explicitly tested. Here we use Approximate Bayesian Computation to refine the previous inferences and test the role of different events in the diversification of two species within P. aurisetus group. We used molecular data from chloroplast DNA and simple sequence repeats loci of P. machrisii and P. aurisetus, the two species with broadest distribution in the complex, in order to test if the diversification in each species was driven mostly by vicariance or by long-dispersal events. We found that both species were affected primarily by vicariance, with a refuge model as the most likely scenario for P. aurisetus and a soft vicariance scenario most probable for P. machrisii. These results emphasize the importance of distributional fragmentation in these species, and add support to the hypothesis of long-term isolation in interglacial refugia previously proposed for the P. aurisetus species complex diversification.

Phylogeographic concordance factors quantify phylogeographic congruence among co-distributed species in the Sarracenia alata pitcher plant system

Jordan D. Satler and Bryan C. Carstens. 2016. DOI: 10.1111/evo.12924

Abstract

Comparative phylogeographic investigations have identified congruent phylogeographic breaks in co-distributed species in nearly every region of the world. The qualitative assessments of phylogeographic patterns traditionally used to identify such breaks, however, are limited because they rely on identifying monophyletic groups across species and do not account for coalescent stochasticity. Only long-standing phylogeographic breaks are likely to be obvious; many species could have had a concerted response to more recent landscape events, yet possess subtle signs of phylogeographic congruence because ancestral polymorphism has not completely sorted. Here we introduce Phylogeographic Concordance Factors (PCFs), a novel method for quantifying phylogeographic congruence across species. We apply this method to the Sarracenia alata pitcher plant system, a carnivorous plant with a diverse array of commensal organisms. We explore whether a group of ecologically associated arthropods have co-diversified with the host pitcher plant, and identify if there is a positive correlation between ecological interaction and PCFs. Results demonstrate that multiple arthropods share congruent phylogeographic breaks with S. alata, and provide evidence that the level of ecological association can be used to predict the degree of similarity in the phylogeographic pattern. This study outlines an approach for quantifying phylogeographic congruence, a central concept in biogeographic research.

Studying the Logone floodplain, Cameroon, as a coupled human and natural system

M Moritz, S Laborde, SC Phang, M Ahmadou, M Durand, A Fernandez;, IM Hamilton, S Kari, B Mark, P Scholte, N Xiao and R Ziebe. 2016. African Journal of Aquatic Science. 41(1): 99–108. http://dx.doi.org/10.2989/16085914.2016.1143799

Abstract

African floodplains are an excellent example of coupled human–natural systems because they exhibit strong interactions among multiple social, ecological, and hydrological systems. The intra-annual and interannual variations in seasonal flooding have direct and indirect impacts on ecosystems and human lives and livelihoods. Coupled human and natural system (CHANS) is a broad conceptual framework that is used to study systems in which human and natural components interact. While there are other conceptual frameworks to study social-ecological systems, the CHANS framework offers a clear way of studying the interactions, called couplings, between human and natural systems. Core features of the framework are the following: human and natural systems are analytically separated; focus is on processes within and couplings between systems; and the goal is to build an integrative, quantitative model of the coupled system. This paper explains the conceptual framework of coupled systems, using the case study of the Logone floodplain in Cameroon. We compare the CHANS framework with other frameworks that have been used to study the same floodplain, and argue for its usefulness in the study of African floodplains.

Cryptic sex? Estimates of genome exchange in unisexual mole salamanders (Ambystoma sp.)

H. Lisle Gibbs, Robert D. Denton. 2016. Mol Ecol. DOI: 10.1111/mec.13662

Abstract

Cryptic sex has been argued to explain the exceptional longevity of certain parthenogenetic vertebrate lineages, yet direct measurements of genetic exchange between sexual and apparently parthenogenetic forms are rare. Female unisexual mole salamanders (Ambystoma sp.) are the oldest known unisexual vertebrate lineage (~5 million years), and one hypothesis for their persistence is that allopolyploid female unisexuals periodically exchange haploid genomes ‘genome exchange’ during gynogenetic reproduction with males from sympatric sexual species. We test this hypothesis by using genome-specific microsatellite DNA markers to estimate the rates of genome exchange between sexual males and unisexual females in two ponds in NE Ohio. We also test the prediction that levels of gene flow should be higher for ‘sympatric’ (sexual males present) genomes in unisexuals compared to ‘allopatric’ (sexual males absent) unisexual genomes. We used a model testing framework in the coalescent-based program MIGRATE-N to compare models where unidirectional gene flow is present and absent between sexual species and unisexuals. As predicted, our results show higher levels of gene flow between sexuals and sympatric unisexual genomes compared to lower (likely artefactual) levels of gene flow between sexuals and allopatric unisexual genomes. Our results provide direct evidence that genome exchange between sexual and unisexual Ambystoma occurs and demonstrate that the magnitude depends on which sexual species are present. The relatively high levels of gene flow suggest that unisexuals must be at a selective advantage over sexual forms so as to avoid extinction due to genetic swamping through genome exchange.

Polyploid unisexual salamanders have higher tissue regeneration rates than diploid sexual relatives.

Saccucci, M. J., Denton, R. D., Holding, M. L. and Gibbs, H. L. 2016.  J Zool. doi:10.1111/jzo.12339

Abstract

Differences in genome composition are known to influence cell division and tissue growth, yet few studies have compared tissue growth between closely related taxa that vary in ploidy and genome composition. Whether cellular mechanisms scale to a functional trait such as tissue regeneration is important for understanding the ecological interactions between polyploids and closely related diploid taxa. We studied regeneration in unisexual Ambystoma salamanders, an ancient unisexual (all-female) lineage in which most individuals are triploids consisting of combinations of two or more distinct genomes from their sexual relatives. We discuss the aspects of haploid genome size and polyploidy that may contribute to variation in tissue regeneration and hypothesize that higher ploidy or variations in genome composition in unisexual Ambystoma would result in increased tissue regeneration compared to diploid sexual relatives, as polyploidy is generally associated with faster limb regeneration. We tested this hypothesis by comparing tail regeneration rates over 4 months between polyploid unisexual salamanders and sympatric diploid sexual salamanders under standardized laboratory conditions. Consistent with our prediction, unisexual Ambystoma regenerated tail tissue at approximately twice the rate of the sexual species. This result provides a physiological difference between unisexual and sexual salaamanders that could influence their coexistence.

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

Matthew L. Holding, James E. Biardi, H. Lisle Gibbs. 2016. Proc. R. Soc. B. 283 20152841. DOI: 10.1098/rspb.2015.2841.

Abstract

Measuring local adaptation can provide insights into how coevolution occurs between predators and prey. Specifically, theory predicts that local adaptation in functionally matched traits of predators and prey will not be detected when coevolution is governed by escalating arms races, whereas it will be present when coevolution occurs through an alternate mechanism of phenotype matching. Here, we analyse local adaptation in venom activity and prey resistance across 12 populations of Northern Pacific rattlesnakes and California ground squirrels, an interaction that has often been described as an arms race. Assays of venom function and squirrel resistance show substantial geographical variation (influenced by site elevation) in both venom metalloproteinase activity and resistance factor effectiveness. We demonstrate local adaptation in the effectiveness of rattlesnake venom to overcoming present squirrel resistance, suggesting that phenotype matching plays a role in the coevolution of these molecular traits. Further, the predator was the locally adapted antagonist in this interaction, arguing that rattlesnakes are evolutionarily ahead of their squirrel prey. Phenotype matching needs to be considered as an important mechanism influencing coevolution between venomous animals and resistant prey.