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1.  Footprints in time: comparative quantitative trait loci mapping of the pitcher-plant mosquito, Wyeomyia smithii 
Identifying regions of the genome contributing to phenotypic evolution often involves genetic mapping of quantitative traits. The focus then turns to identifying regions of ‘major’ effect, overlooking the observation that traits of ecological or evolutionary relevance usually involve many genes whose individual effects are small but whose cumulative effect is large. Herein, we use the power of fully interfertile natural populations of a single species of mosquito to develop three quantitative trait loci (QTL) maps: one between two post-glacially diverged populations and two between a more ancient and a post-glacial population. All demonstrate that photoperiodic response is genetically a highly complex trait. Furthermore, we show that marker regressions identify apparently ‘non-significant’ regions of the genome not identified by composite interval mapping, that the perception of the genetic basis of adaptive evolution is crucially dependent upon genetic background and that the genetic basis for adaptive evolution of photoperiodic response is highly variable within contemporary populations as well as between anciently diverged populations.
PMCID: PMC3479738  PMID: 23015622
QTL map; marker regression; photoperiodism; genomics; RAD-seq; geological time
2.  Replicate Phylogenies and Post-Glacial Range Expansion of the Pitcher-Plant Mosquito, Wyeomyia smithii, in North America 
PLoS ONE  2013;8(9):e72262.
Herein we tested the repeatability of phylogenetic inference based on high throughput sequencing by increased taxon sampling using our previously published techniques in the pitcher-plant mosquito, Wyeomyia smithii in North America. We sampled 25 natural populations drawn from different localities nearby 21 previous collection localities and used these new data to construct a second, independent phylogeny, expressly to test the reproducibility of phylogenetic patterns. Comparison of trees between the two data sets based on both maximum parsimony and maximum likelihood with Bayesian posterior probabilities showed close correspondence in the grouping of the most southern populations into clear clades. However, discrepancies emerged, particularly in the middle of W. smithii's current range near the previous maximum extent of the Laurentide Ice Sheet, especially concerning the most recent common ancestor to mountain and northern populations. Combining all 46 populations from both studies into a single maximum parsimony tree and taking into account the post-glacial historical biogeography of associated flora provided an improved picture of W. smithii's range expansion in North America. In a more general sense, we propose that extensive taxon sampling, especially in areas of known geological disruption is key to a comprehensive approach to phylogenetics that leads to biologically meaningful phylogenetic inference.
PMCID: PMC3765167  PMID: 24039746
3.  Conservation of the photoperiodic neuroendocrine axis among vertebrates: evidence from the teleost fish, Gasterosteus aculeatus 
Photoperiod, or length of day, has a predictable annual cycle, making it an important cue for the timing of seasonal behavior and development in many organisms. Photoperiod is widely used among temperate and polar animals to regulate the timing of sexual maturation. The proper sensing and interpretation of photoperiod can be tightly tied to an organism’s overall fitness. In photoperiodic mammals and birds the thyroid hormone pathway initiates sexual maturation, but the degree to which this pathway is conserved across other vertebrates is not well known. We use the threespine stickleback Gasterosteus aculeatus, as a representative teleost to quantify the photoperiodic response of key genes in the thyroid hormone pathway under controlled laboratory conditions. We find that the photoperiodic responses of the hormones are largely consistent amongst multiple populations, although differences suggest physiological adaptation to various climates. We conclude that the thyroid hormone pathway initiates sexual maturation in response to photoperiod in G. aculeatus, and our results show that more components of this pathway are conserved among mammals, birds, and teleost fish than was previously known. However, additional endocrinology, cell biology and molecular research will be required to define precisely which aspects of the pathway are conserved across vertebrates.
PMCID: PMC3389224  PMID: 22504272
Thyroid hormone; Thyroid stimulating hormone; Gonadotropin releasing hormone; Lutenizing hormone; Threespine stickleback; photoperiodism
4.  Testing for causality in covarying traits: genes and latitude in a molecular world 
Molecular ecology  2011;20(12):2471–6.
Many traits are assumed to have a causal (necessary) relationship with one another because of their common covariation with a physiological, ecological, or geographical factor. Herein we demonstrate a straightforward test for inferring causality using residuals from regression of the traits with the common factor. We illustrate this test using the covariation with latitude of a proxy for the circadian clock and a proxy for the photoperiodic timer in Drosophila and salmon. A negative result of this test means that further discussion of the adaptive significance of a causal connection between the covarying traits is unwarranted. A positive result of this test provides a point of departure that can then be used as a platform from which to determine experimentally the underlying functional connections and only then to discuss their adaptive significance.
PMCID: PMC3362484  PMID: 21595769
covariation; ecogeographic gradient; circadian; photoperiodism; salmon; Drosophila
5.  Circadian clock genes, ovarian development and diapause 
BMC Biology  2010;8:115.
Insects, like most organisms, have an internal circadian clock that oscillates with a daily rhythmicity, and a timing mechanism that mediates seasonal events, including diapause. In research published in BMC Biology, Ikeno et al. show that downregulation of the circadian clock genes period and cycle affects expression of ovarian diapause in the insect Riptortus pedestris. They interpret these important results as support for Erwin Bünning's (1936) hypothesis that the circadian clock constitutes the basis of photoperiodism. However, their observations could also be the result of pleiotropic effects of the individual clock genes.
See research article
PMCID: PMC2933584  PMID: 20828372
6.  Microarrays Reveal Early Transcriptional Events during the Termination of Larval Diapause in Natural Populations of the Mosquito, Wyeomyia smithii 
PLoS ONE  2010;5(3):e9574.
The mosquito Wyeomyia smithii overwinters in a larval diapause that is initiated, maintained and terminated by day length (photoperiod). We use a forward genetic approach to investigate transcriptional events involved in the termination of diapause following exposure to long-days.
Methods/Principal Findings
We incorporate a novel approach that compares two populations that differentially respond to a single day length. We identify 30 transcripts associated with differential response to day length. Most genes with a previously annotated function are consistent with their playing a role in the termination of diapause, in downstream developmental events, or in the transition from potentially oxygen-poor to oxygen-rich environments. One gene emerges from three separate forward genetic screens as a leading candidate for a gene contributing to the photoperiodic timing mechanism itself (photoperiodic switch). We name this gene photoperiodic response gene 1 (ppdrg1). WsPpdrg1 is up-regulated under long-day response conditions, is located under a QTL for critical photoperiod and is associated with critical photoperiod after 25 generations of recombination from a cross between extreme phenotypes.
Three independent forward genetic approaches identify WsPpdrg1 as a gene either involved in the photoperiodic switch mechanism or very tightly linked to a gene that is. We conclude that continued forward genetic approaches will be central to understanding not only the molecular basis of photoperiodism and diapause, but also the evolutionary potential of temperate and polar animal populations when confronted with rapid climate change.
PMCID: PMC2832704  PMID: 20221437
7.  Cloning the Professor, an Alternative to Ineffective Teaching in a Large Course 
CBE Life Sciences Education  2009;8(3):252-263.
Pedagogical strategies have been experimentally applied in large-enrollment biology courses in an attempt to amplify what teachers do best in effecting deep learning, thus more closely approximating a one-on-one interaction with students. Carefully orchestrated in-class formative assessments were conducted to provide frequent, high-quality feedback that allows students to accurately diagnose the current state of their understanding of fundamental biological concepts and make specific plans to remedy any deficiencies. Teachers can also assume responsibility to guide out-of-class study among classmates by promoting Elaborative Questioning, an inquiry exchange that permits misconceptions to be identified and corrected and that promotes long-lasting metacognitive and analytical thinking skills. Data are presented that demonstrate the positive impact of these innovations on student performance and affect.
PMCID: PMC2736028  PMID: 19723819
8.  Rethinking Exams and Letter Grades: How Much Can Teachers Delegate to Students? 
CBE— Life Sciences Education  2006;5(3):270-280.
In this article we report a 3-yr study of a large-enrollment Cell Biology course focused on developing student skill in scientific reasoning and data interpretation. Specifically, the study tested the hypothesis that converting the role of exams from summative grading devices to formative tools would increase student success in acquiring those skills. Traditional midterm examinations were replaced by weekly assessments administered under test-like conditions and followed immediately by extensive self, peer, and instructor feedback. Course grades were criterion based and derived using data from the final exam. To alleviate anxiety associated with a single grading instrument, students were given the option of informing the grading process with evidence from weekly assessments. A comparative analysis was conducted to determine the impact of these design changes on both performance and measures of student affect. Results at the end of each year were used to inform modifications to the course in subsequent years. Significant improvements in student performance and attitudes were observed as refinements were implemented. The findings from this study emphasized the importance of prolonging student opportunity and motivation to improve by delaying grade decisions, providing frequent and immediate performance feedback, and designing that feedback to be maximally formative and minimally punitive.
PMCID: PMC1618686  PMID: 17012219
9.  Teaching Cell Biology in the Large-Enrollment Classroom: Methods to Promote Analytical Thinking and Assessment of Their Effectiveness 
Cell Biology Education  2003;2:180-194.
A large-enrollment, undergraduate cellular biology lecture course is described whose primary goal is to help students acquire skill in the interpretation of experimental data. The premise is that this kind of analytical reasoning is not intuitive for most people and, in the absence of hands-on laboratory experience, will not readily develop unless instructional methods and examinations specifically designed to foster it are employed. Promoting scientific thinking forces changes in the roles of both teacher and student. We describe didactic strategies that include directed practice of data analysis in a workshop format, active learning through verbal and written communication, visualization of abstractions diagrammatically, and the use of ancillary small-group mentoring sessions with faculty. The implications for a teacher in reducing the breadth and depth of coverage, becoming coach instead of lecturer, and helping students to diagnose cognitive weaknesses are discussed. In order to determine the efficacy of these strategies, we have carefully monitored student performance and have demonstrated a large gain in a pre- and posttest comparison of scores on identical problems, improved test scores on several successive midterm examinations when the statistical analysis accounts for the relative difficulty of the problems, and higher scores in comparison to students in a control course whose objective was information transfer, not acquisition of reasoning skills. A novel analytical index (student mobility profile) is described that demonstrates that this improvement was not random, but a systematic outcome of the teaching/learning strategies employed. An assessment of attitudes showed that, in spite of finding it difficult, students endorse this approach to learning, but also favor curricular changes that would introduce an analytical emphasis earlier in their training.
PMCID: PMC192442  PMID: 14506506
Rasch analysis; item response theory; student outcome; student attitude; student confidence

Results 1-9 (9)