Kevin J. Emerson

Resolving postglacial phylogeography using high-throughput sequencing

The distinction between model and nonmodel organisms is becoming increasingly blurred. High-throughput, second-generation sequencing approaches are being applied to organisms based on their interesting ecological, physiological, developmental, or evolutionary properties and not on the depth of genetic information available for them. Here, we illustrate this point using a low-cost, efficient technique to determine the fine-scale phylogenetic relationships among recently diverged populations in a species. This application of restriction site-associated DNA tags (RAD tags) reveals previously unresolved genetic structure and direction of evolution in the pitcher plant mosquito, Wyeomyia smithii, from a southern Appalachian Mountain refugium following recession of the Laurentide Ice Sheet at 22,000–19,000 B.P. The RAD tag method can be used to identify detailed patterns of phylogeography in any organism regardless of existing genomic data, and, more broadly, to identify incipient speciation and genome-wide variation in natural populations in general.

Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause

Understanding gene interaction and pleiotropy are long-standing goals of developmental and evolutionary biology. We examine the genetic control of diapause in insects and show how the failure to recognize the difference between modular and gene pleiotropy has confounded our understanding of the genetic basis of this important phenotype. This has led to complications in understanding the role of the circadian clock in the control of diapause in Drosophila and other insects. We emphasize three successive modules - each containing functionally related genes - that lead to diapause: photoperiodism, hormonal events and diapause itself. Understanding the genetic basis for environmental control of diapause has wider implications for evolutionary response to rapid climate change and for the opportunity to observe evolutionary change in contemporary time.

EPISTASIS AND DOMINANCE: EVIDENCE FOR DIFFERENTIAL EFFECTS IN LIFE-HISTORY VERSUS MORPHOLOGICAL TRAITS

Abstract Dominance and epistatic effects are predicted to be larger in life‐history than in morphological traits. We test these predictions using published results from line cross analyses. We find that dominance is found in more than 95% of traits, regardless of the type of trait, but that the magnitude of the effect in relation to the additive effect is much greater in life‐history than in morphological traits. Epistatic effects were detected more often in life‐history than in morphological traits (79% and 67%, respectively). We also test for a difference in the magnitude of the effects by comparing the ratio of the nonadditive components separately to the additive component. For both dominance and epistatic components, the ratio of the nonadditive component to additive effects in life‐history traits is approximately twice as large as that for morphological traits.

CONCORDANCE OF THE CIRCADIAN CLOCK WITH THE ENVIRONMENT IS NECESSARY TO MAXIMIZE FITNESS IN NATURAL POPULATIONS

Abstract The ubiquity of endogenous, circadian (daily) clocks among eukaryotes has long been held as evidence that they serve an adaptive function, usually cited as the ability to properly time biological events in concordance with the daily cycling of the environment. Herein we test directly whether fitness is a function of the matching of the period of an organisms circadian clock with that of its environment. We find that fitness, measured as the per capita expectation of future offspring, a composite measure of fitness incorporating both survivorship and reproduction, is maximized in environments that are integral multiples of the period of the organisms circadian clock. Hence, we show that organisms require temporal concordance between their internal circadian clocks and their external environment to maximize fitness and thus the long-held assumption is true that, having evolved in a 24-h world, circadian clocks are adaptive.

Microarrays Reveal Early Transcriptional Events during the Termination of Larval Diapause in Natural Populations of the Mosquito, Wyeomyia smithii

Background 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. Conclusions 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.

Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster

Drosophila melanogaster from Australia, Europe and North America enter an adult ovarian dormancy in response to short days and low temperatures. The independent effects of temperature and day length in the determination of dormancy have been examined only in one long-established laboratory line (Canton-S). In all other studies of natural or laboratory populations, dormancy has been assessed at either a single short day or a single moderately low temperature. Herein, we determine the relative roles of temperature, photoperiod, and their interaction in the control of ovarian dormancy in D. melanogaster from two natural populations representing latitudinal extremes in eastern North America (Florida at 27°N and Maine at 44°N). In both natural populations, temperature is the main determinant of dormancy, alone explaining 67% of the total variation among replicate isofemale lines, whereas photoperiod has no significant effect. We conclude that ovarian dormancy in D. melanogaster is a temperature-initiated syndrome of winter-tolerant traits that represents an adaptive phenotypic plasticity in temperate seasonal environments.

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.

StrAuto: automation and parallelization of STRUCTURE analysis

BackgroundPopulation structure inference using the software STRUCTURE has become an integral part of population genetic studies covering a broad spectrum of taxa including humans. The ever-expanding size of genetic data sets poses computational challenges for this analysis. Although at least one tool currently implements parallel computing to reduce computational overload of this analysis, it does not fully automate the use of replicate STRUCTURE analysis runs required for downstream inference of optimal K. There is pressing need for a tool that can deploy population structure analysis on high performance computing clusters.ResultsWe present an updated version of the popular Python program StrAuto, to streamline population structure analysis using parallel computing. StrAuto implements a pipeline that combines STRUCTURE analysis with the Evanno ΔK analysis and visualization of results using STRUCTURE HARVESTER. Using benchmarking tests, we demonstrate that StrAuto significantly reduces the computational time needed to perform iterative STRUCTURE analysis by distributing runs over two or more processors.ConclusionStrAuto is the first tool to integrate STRUCTURE analysis with post-processing using a pipeline approach in addition to implementing parallel computation – a set up ideal for deployment on computing clusters. StrAuto is distributed under the GNU GPL (General Public License) and available to download from http://strauto.popgen.org.

Extrinsic light:dark cycles, rather than endogenous circadian cycles, affect the photoperiodic counter in the pitcher-plant mosquito, Wyeomyia smithii

A wide diversity of organisms use photoperiod (daylength) as an environmental cue to anticipate the changing seasons and to time various life-history events such as dormancy and migration. Photoperiodic time measurement consists of two main components, (1) the photoperiodic timer that discriminates between long and short days, and (2) the photoperiodic counter that accumulates and stores information from the timer and then induces the phenotypic output. Herein, we use extended night treatments to show that light is necessary to accumulate photoperiodic information across the geographic range of the mosquito, Wyeomyia smithii and that the photoperiodic counter counts extrinsic (external) light:dark cycles and not endogenous (internal) circadian cycles.

Replicate Phylogenies and Post-Glacial Range Expansion of the Pitcher-Plant Mosquito, Wyeomyia smithii, in North America

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. smithiis 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. smithiis 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.