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Background: Meiotic recombination has traditionally been explained based on the structural requirement to stabilize homologous chromosome pairs to ensure their proper meiotic segregation. Competing hypotheses seek to explain the emerging findings of significant heterogeneity in recombination rates within and between genomes, but intraspecific comparisons of genome-wide recombination patterns are rare.

Background: Meiotic recombination has traditionally been explained based on the structural requirement to stabilize homologous chromosome pairs to ensure their proper meiotic segregation. Competing hypotheses seek to explain the emerging findings of significant heterogeneity in recombination rates within and between genomes, but intraspecific comparisons of genome-wide recombination patterns are rare. The honey bee (Apis mellifera) exhibits the highest rate of genomic recombination among multicellular animals with about five cross-over events per chromatid.

Results: Here, we present a comparative analysis of recombination rates across eight genetic linkage maps of the honey bee genome to investigate which genomic sequence features are correlated with recombination rate and with its variation across the eight data sets, ranging in average marker spacing ranging from 1 Mbp to 120 kbp. Overall, we found that GC content explained best the variation in local recombination rate along chromosomes at the analyzed 100 kbp scale. In contrast, variation among the different maps was correlated to the abundance of microsatellites and several specific tri- and tetra-nucleotides.

Conclusions: The combined evidence from eight medium-scale recombination maps of the honey bee genome suggests that recombination rate variation in this highly recombining genome might be due to the DNA configuration instead of distinct sequence motifs. However, more fine-scale analyses are needed. The empirical basis of eight differing genetic maps allowed for robust conclusions about the correlates of the local recombination rates and enabled the study of the relation between DNA features and variability in local recombination rates, which is particularly relevant in the honey bee genome with its exceptionally high recombination rate.

ContributorsRoss, Caitlin R. (Author) / DeFelice, Dominick S. (Author) / Hunt, Greg J. (Author) / Ihle, Kate (Author) / Amdam, Gro (Author) / Rueppell, Olav (Author) / College of Liberal Arts and Sciences (Contributor)
Created2015-02-21
Description

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.

Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.

Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

ContributorsSadd, Ben M. (Author) / Barribeau, Seth M. (Author) / Bloch, Guy (Author) / de Graaf, Dirk C. (Author) / Dearden, Peter (Author) / Elsik, Christine G. (Author) / Gadau, Juergen (Author) / Grimmelikhuijzen, Cornelis J. P. (Author) / Hasselmann, Martin (Author) / Lozier, Jeffrey D. (Author) / Robertson, Hugh M. (Author) / Smagghe, Guy (Author) / Stolle, Eckart (Author) / Van Vaerenbergh, Matthias (Author) / Waterhouse, Robert M. (Author) / Bornberg-Bauer, Erich (Author) / Klasberg, Steffen (Author) / Bennett, Anna K. (Author) / Camara, Francisco (Author) / Guigo, Roderic (Author) / Hoff, Katharina (Author) / Mariotti, Marco (Author) / Munoz-Torres, Monica (Author) / Murphy, Terence (Author) / Santesmasses, Didac (Author) / Amdam, Gro (Author) / Beckers, Matthew (Author) / Beye, Martin (Author) / Biewer, Matthias (Author) / Bitondi, Marcia MG (Author) / Blaxter, Mark L. (Author) / Bourke, Andrew FG (Author) / Brown, Mark JF (Author) / Buechel, Severine D. (Author) / Cameron, Rossanah (Author) / Cappelle, Kaat (Author) / Carolan, James C. (Author) / Christiaens, Olivier (Author) / Ciborowski, Kate L. (Author) / Clarke, David F. (Author) / Colgan, Thomas J. (Author) / Collins, David H. (Author) / Cridge, Andrew G. (Author) / Dalmay, Tamas (Author) / Dreier, Stephanie (Author) / du Plessis, Louis (Author) / Duncan, Elizabeth (Author) / Erler, Silvio (Author) / Evans, Jay (Author) / Falcon, Talgo (Author) / Flores, Kevin (Author) / Freitas, Flavia CP (Author) / Fuchikawa, Taro (Author) / Gempe, Tanja (Author) / Hartfelder, Klaus (Author) / Hauser, Frank (Author) / Helbing, Sophie (Author) / Humann, Fernanda (Author) / Irvine, Frano (Author) / Jermiin, Lars S (Author) / Johnson, Claire E. (Author) / Johnson, Reed M (Author) / Jones, Andrew K. (Author) / Kadowaki, Tatsuhiko (Author) / Kidner, Jonathan H. (Author) / Koch, Vasco (Author) / Kohler, Arian (Author) / Kraus, F. Bernhard (Author) / Lattorff, H. Michael G. (Author) / Leask, Megan (Author) / Lockett, Gabrielle A. (Author) / Mallon, Eamonn B. (Author) / Marco Antonio, David S. (Author) / Marxer, Monika (Author) / Meeus, Ivan (Author) / Moritz, Robin FA (Author) / Nair, Ajay (Author) / Napflin, Kathrin (Author) / Nissen, Inga (Author) / Niu, Jinzhi (Author) / Nunes, Francis MF (Author) / Oakeshott, John G. (Author) / Osborne, Amy (Author) / Otte, Marianne (Author) / Pinheiro, Daniel G. (Author) / Rossie, Nina (Author) / Rueppell, Olav (Author) / Santos, Carolina G (Author) / Schmid-Hempel, Regula (Author) / Schmitt, Bjorn D. (Author) / Schulte, Christina (Author) / Simoes, Zila LP (Author) / Soares, Michelle PM (Author) / Swevers, Luc (Author) / Winnebeck, Eva C. (Author) / Wolschin, Florian (Author) / Yu, Na (Author) / Zdobnov, Evgeny M (Author) / Aqrawi, Peshtewani K (Author) / Blakenburg, Kerstin P (Author) / Coyle, Marcus (Author) / Francisco, Liezl (Author) / Hernandez, Alvaro G. (Author) / Holder, Michael (Author) / Hudson, Matthew E. (Author) / Jackson, LaRonda (Author) / Jayaseelan, Joy (Author) / Joshi, Vandita (Author) / Kovar, Christie (Author) / Lee, Sandra L. (Author) / Mata, Robert (Author) / Mathew, Tittu (Author) / Newsham, Irene F. (Author) / Ngo, Robin (Author) / Okwuonu, Geoffrey (Author) / Pham, Christopher (Author) / Pu, Ling-Ling (Author) / Saada, Nehad (Author) / Santibanez, Jireh (Author) / Simmons, DeNard (Author) / Thornton, Rebecca (Author) / Venkat, Aarti (Author) / Walden, Kimberly KO (Author) / Wu, Yuan-Qing (Author) / Debyser, Griet (Author) / Devreese, Bart (Author) / Asher, Claire (Author) / Blommaert, Julie (Author) / Chipman, Ariel D. (Author) / Chittka, Lars (Author) / Fouks, Bertrand (Author) / Liu, Jisheng (Author) / O'Neill, Meaghan P (Author) / Sumner, Seirian (Author) / Puiu, Daniela (Author) / Qu, Jiaxin (Author) / Salzberg, Steven L (Author) / Scherer, Steven E (Author) / Muzny, Donna M. (Author) / Richards, Stephen (Author) / Robinson, Gene E (Author) / Gibbs, Richard A. (Author) / Schmid-Hempel, Paul (Author) / Worley, Kim C (Author) / College of Liberal Arts and Sciences (Contributor)
Created2015-04-24
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Description

Honeybee workers are essentially sterile female helpers that make up the majority of individuals in a colony. Workers display a marked change in physiology when they transition from in-nest tasks to foraging. Recent technological advances have made it possible to unravel the metabolic modifications associated with this transition. Previous studies

Honeybee workers are essentially sterile female helpers that make up the majority of individuals in a colony. Workers display a marked change in physiology when they transition from in-nest tasks to foraging. Recent technological advances have made it possible to unravel the metabolic modifications associated with this transition. Previous studies have revealed extensive remodeling of brain, thorax, and hypopharyngeal gland biochemistry. However, data on changes in the abdomen is scarce. To narrow this gap we investigated the proteomic composition of abdominal tissue in the days typically preceding the onset of foraging in honeybee workers.

In order to get a broader representation of possible protein dynamics, we used workers of two genotypes with differences in the age at which they initiate foraging. This approach was combined with RNA interference-mediated downregulation of an insulin/insulin-like signaling component that is central to foraging behavior, the insulin receptor substrate (irs), and with measurements of glucose and lipid levels.
Our data provide new insight into the molecular underpinnings of phenotypic plasticity in the honeybee, invoke parallels with vertebrate metabolism, and support an integrated and irs-dependent association of carbohydrate and lipid metabolism with the transition from in-nest tasks to foraging.

ContributorsChan, Queenie W. T. (Author) / Mutti, Navdeep (Author) / Foster, Leonard J. (Author) / Kocher, Sarah D. (Author) / Amdam, Gro (Author) / Wolschin, Florian (Author) / College of Liberal Arts and Sciences (Contributor)
Created2011-09-28
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Description

Background: Gene bodies are the most evolutionarily conserved targets of DNA methylation in eukaryotes. However, the regulatory functions of gene body DNA methylation remain largely unknown. DNA methylation in insects appears to be primarily confined to exons. Two recent studies in Apis mellifera (honeybee) and Nasonia vitripennis (jewel wasp) analyzed transcription

Background: Gene bodies are the most evolutionarily conserved targets of DNA methylation in eukaryotes. However, the regulatory functions of gene body DNA methylation remain largely unknown. DNA methylation in insects appears to be primarily confined to exons. Two recent studies in Apis mellifera (honeybee) and Nasonia vitripennis (jewel wasp) analyzed transcription and DNA methylation data for one gene in each species to demonstrate that exon-specific DNA methylation may be associated with alternative splicing events. In this study we investigated the relationship between DNA methylation, alternative splicing, and cross-species gene conservation on a genome-wide scale using genome-wide transcription and DNA methylation data.

Results: We generated RNA deep sequencing data (RNA-seq) to measure genome-wide mRNA expression at the exon- and gene-level. We produced a de novo transcriptome from this RNA-seq data and computationally predicted splice variants for the honeybee genome. We found that exons that are included in transcription are higher methylated than exons that are skipped during transcription. We detected enrichment for alternative splicing among methylated genes compared to unmethylated genes using fisher’s exact test. We performed a statistical analysis to reveal that the presence of DNA methylation or alternative splicing are both factors associated with a longer gene length and a greater number of exons in genes. In concordance with this observation, a conservation analysis using BLAST revealed that each of these factors is also associated with higher cross-species gene conservation.

Conclusions: This study constitutes the first genome-wide analysis exhibiting a positive relationship between exon-level DNA methylation and mRNA expression in the honeybee. Our finding that methylated genes are enriched for alternative splicing suggests that, in invertebrates, exon-level DNA methylation may play a role in the construction of splice variants by positively influencing exon inclusion during transcription. The results from our cross-species homology analysis suggest that DNA methylation and alternative splicing are genetic mechanisms whose utilization could contribute to a longer gene length and a slower rate of gene evolution.

ContributorsFlores, Kevin (Author) / Wolschin, Florian (Author) / Corneveaux, Jason J. (Author) / Allen, April N. (Author) / Huentelman, Matthew J. (Author) / Amdam, Gro (Author) / College of Liberal Arts and Sciences (Contributor)
Created2012-09-15
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Description

In spite of well-documented health benefits of vegetarian diets, less is known regarding the effects of these diets on athletic performance. In this cross-sectional study, we compared elite vegetarian and omnivore adult endurance athletes for maximal oxygen uptake (VO2 max) and strength. Twenty-seven vegetarian (VEG) and 43 omnivore (OMN) athletes

In spite of well-documented health benefits of vegetarian diets, less is known regarding the effects of these diets on athletic performance. In this cross-sectional study, we compared elite vegetarian and omnivore adult endurance athletes for maximal oxygen uptake (VO2 max) and strength. Twenty-seven vegetarian (VEG) and 43 omnivore (OMN) athletes were evaluated using VO2 max testing on the treadmill, and strength assessment using a dynamometer to determine peak torque for leg extensions. Dietary data were assessed using detailed seven-day food logs. Although total protein intake was lower among vegetarians in comparison to omnivores, protein intake as a function of body mass did not differ by group (1.2 ± 0.3 and 1.4 ± 0.5 g/kg body mass for VEG and OMN respectively, p = 0.220). VO2 max differed for females by diet group (53.0 ± 6.9 and 47.1 ± 8.6 mL/kg/min for VEG and OMN respectively, p < 0.05) but not for males (62.6 ± 15.4 and 55.7 ± 8.4 mL/kg/min respectively). Peak torque did not differ significantly between diet groups. Results from this study indicate that vegetarian endurance athletes’ cardiorespiratory fitness was greater than that for their omnivorous counterparts, but that peak torque did not differ between diet groups. These data suggest that vegetarian diets do not compromise performance outcomes and may facilitate aerobic capacity in athletes.

ContributorsLynch, Heidi (Author) / Wharton, Christopher (Author) / Johnston, Carol (Author) / College of Health Solutions (Contributor)
Created2016-11-15
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Description

Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of

Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of immune elicitors. Using the honey bee, Apis mellifera, model system, we demonstrate with microscopy and western blotting that vitellogenin binds to bacteria, both Paenibacillus larvae – the gram-positive bacterium causing American foulbrood disease – and to Escherichia coli that represents gram-negative bacteria. Next, we verify that vitellogenin binds to pathogen-associated molecular patterns; lipopolysaccharide, peptidoglycan and zymosan, using surface plasmon resonance. We document that vitellogenin is required for transport of cell-wall pieces of E. coli into eggs by imaging tissue sections. These experiments identify vitellogenin, which is distributed widely in oviparous species, as the carrier of immune-priming signals. This work reveals a molecular explanation for trans-generational immunity in insects and a previously undescribed role for vitellogenin.

ContributorsSalmela, Heli (Author) / Amdam, Gro (Author) / Freitak, Dalial (Author) / College of Liberal Arts and Sciences (Contributor)
Created2015-07-31
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Description

Background: Peanut consumption favorably influences satiety. This study examined the acute effect of peanut versus grain bar preloads on postmeal satiety and glycemia in healthy adults and the long-term effect of these meal preloads on body mass in healthy overweight adults.

Methods: In the acute crossover trial (n = 15; 28.4 ± 2.9 y; 23.1 ± 0.9

Background: Peanut consumption favorably influences satiety. This study examined the acute effect of peanut versus grain bar preloads on postmeal satiety and glycemia in healthy adults and the long-term effect of these meal preloads on body mass in healthy overweight adults.

Methods: In the acute crossover trial (n = 15; 28.4 ± 2.9 y; 23.1 ± 0.9 kg/m2), the preload (isoenergetic peanut or grain bar with water, or water alone) was followed after 60 min with ingestion of a standardized glycemic test meal. Satiety and blood glucose were assessed immediately prior to the preload and to the test meal, and for two hours postmeal at 30-min intervals. In the parallel-arm, randomized trial (n = 44; 40.5 ± 1.6 y, 31.8 ± 0.9 kg/m2), the peanut or grain bar preload was consumed one hour prior to the evening meal for eight weeks. Body mass was measured at 2-week intervals, and secondary endpoints included blood hemoglobin A1c and energy intake as assessed by 3-d diet records collected at pre-trial and trial weeks 1 and 8.

Results: Satiety was elevated in the postprandial period following grain bar ingestion in comparison to peanut or water ingestion (p = 0.001, repeated-measures ANOVA). Blood glucose was elevated one hour after ingestion of the grain bar as compared to the peanut or water treatments; yet, total glycemia did not vary between treatments in the two hour postprandial period. In the 8-week trial, body mass was reduced for the grain bar versus peanut groups after eight weeks (−1.3 ± 0.4 kg versus −0.2 ± 0.3 kg, p = 0.033, analysis of covariance). Energy intake was reduced by 458 kcal/d in the first week of the trial for the grain bar group as compared to the peanut group (p = 0.118). Hemoglobin A1c changed significantly between groups during the trial (−0.25 ± 0.07% and −0.18 ± 0.12% for the grain bar and peanut groups respectively, p = 0.001).

Conclusions: Compared to an isoenergetic peanut preload, consumption of a grain bar preload one hour prior to a standardized meal significantly raised postmeal satiety. Moreover, consumption of the grain bar prior to the evening meal was associated with significant weight loss over time suggesting that glycemic carbohydrate ingestion prior to meals may be a weight management strategy.

ContributorsJohnston, Carol (Author) / Catherine, Trier (Author) / Fleming, Katie (Author) / College of Health Solutions (Contributor)
Created2013-03-27
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Description

Background: Height is an important health assessment measure with many applications. In the medical practice and in research settings, height is typically measured with a stadiometer. Although lasers are commonly used by health professionals for measurement including facial imaging, corneal thickness, and limb length, it has not been utilized for

Background: Height is an important health assessment measure with many applications. In the medical practice and in research settings, height is typically measured with a stadiometer. Although lasers are commonly used by health professionals for measurement including facial imaging, corneal thickness, and limb length, it has not been utilized for measuring height. The purpose of this feasibility study was to examine the ease and accuracy of a laser device for measuring height in children and adults.

Findings: In immediate succession, participant height was measured in triplicate using a stadiometer followed by the laser device. Measurement error for the laser device was significantly higher than that for the stadiometer (0.35 and 0.20 cm respectively). However, the measurement techniques were highly correlated (r2 = 0.998 and 0.990 for the younger [<12 y, n = 25] and older [≥12 y, n = 100] participants respectively), and the estimated reliability between measurement techniques was 0.999 (ICC; 95 % CI: 0.998,1.000) and 0.995 (ICC; 95 % CI: 0.993,0.997) for the younger and older groups respectively. The average differences between the two styles of measurement (e.g., stadiometer minus laser) were significantly different from zero: +0.93 and +0.45 cm for the younger and older groups respectively.

Conclusions: These data demonstrate that laser technology can be adapted to measure height in children and adults. Although refinement is needed, the laser device for measuring height merits further development.

ContributorsMayol-Kreiser, Sandra (Author) / Garcia-Turner, Vanessa (Author) / Johnston, Carol (Author) / College of Health Solutions (Contributor)
Created2015-08-31
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Description

Background: Phosphatase and TENsin (PTEN) homolog is a negative regulator that takes part in IIS (insulin/insulin-like signaling) and Egfr (epidermal growth factor receptor) activation in Drosophila melanogaster. IIS and Egfr signaling events are also involved in the developmental process of queen and worker differentiation in honey bees (Apis mellifera). Here, we

Background: Phosphatase and TENsin (PTEN) homolog is a negative regulator that takes part in IIS (insulin/insulin-like signaling) and Egfr (epidermal growth factor receptor) activation in Drosophila melanogaster. IIS and Egfr signaling events are also involved in the developmental process of queen and worker differentiation in honey bees (Apis mellifera). Here, we characterized the bee PTEN gene homologue for the first time and begin to explore its potential function during bee development and adult life.

Results: Honey bee PTEN is alternatively spliced, resulting in three splice variants. Next, we show that the expression of PTEN can be down-regulated by RNA interference (RNAi) in the larval stage, when female caste fate is determined. Relative to controls, we observed that RNAi efficacy is dependent on the amount of PTEN dsRNA that is delivered to larvae. For larvae fed queen or worker diets containing a high amount of PTEN dsRNA, PTEN knockdown was significant at a whole-body level but lethal. A lower dosage did not result in a significant gene down-regulation. Finally, we compared same-aged adult workers with different behavior: nursing vs. foraging. We show that between nurses and foragers, PTEN isoforms were differentially expressed within brain, ovary and fat body tissues. All isoforms were expressed at higher levels in the brain and ovaries of the foragers. In fat body, isoform B was expressed at higher level in the nurse bees.

Conclusion: Our results suggest that PTEN plays a central role during growth and development in queen- and worker-destined honey bees. In adult workers, moreover, tissue-specific patterns of PTEN isoform expression are correlated with differences in complex division of labor between same-aged individuals. Therefore, we propose that knowledge on the roles of IIS and Egfr activity in developmental and behavioral control may increase through studies of how PTEN functions can impact bee social phenotypes.

ContributorsMutti, Navdeep (Author) / Wang, Ying (Author) / Kaftanoglu, Osman (Author) / Amdam, Gro (Author) / College of Liberal Arts and Sciences (Contributor)
Created2011-07-14
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Description

In vitro rearing is an important and useful tool for honey bee (Apis mellifera L.) studies. However, it often results in intercastes between queens and workers, which are normally are not seen in hive-reared bees, except when larvae older than three days are grafted for queen rearing. Morphological classification (queen

In vitro rearing is an important and useful tool for honey bee (Apis mellifera L.) studies. However, it often results in intercastes between queens and workers, which are normally are not seen in hive-reared bees, except when larvae older than three days are grafted for queen rearing. Morphological classification (queen versus worker or intercastes) of bees produced by this method can be subjective and generally depends on size differences. Here, we propose an alternative method for caste classification of female honey bees reared in vitro, based on weight at emergence, ovariole number, spermatheca size and size and shape, and features of the head, mandible and basitarsus. Morphological measurements were made with both traditional morphometric and geometric morphometrics techniques. The classifications were performed by principal component analysis, using naturally developed queens and workers as controls. First, the analysis included all the characters. Subsequently, a new analysis was made without the information about ovariole number and spermatheca size. Geometric morphometrics was less dependent on ovariole number and spermatheca information for caste and intercaste identification. This is useful, since acquiring information concerning these reproductive structures requires time-consuming dissection and they are not accessible when abdomens have been removed for molecular assays or in dried specimens. Additionally, geometric morphometrics divided intercastes into more discrete phenotype subsets. We conclude that morphometric geometrics are superior to traditional morphometrics techniques for identification and classification of honey bee castes and intermediates.

ContributorsDe Souza, Daiana A. (Author) / Wang, Ying (Author) / Kaftanoglu, Osman (Author) / De Jong, David (Author) / Amdam, Gro (Author) / Goncalves, Lionel S. (Author) / Francoy, Tiago M. (Author) / College of Liberal Arts and Sciences (Contributor)
Created2015-04-20