Quantitative Trait Loci Associated with Photoperiodic Response and Stage of Diapause in the Pitcher-Plant Mosquito, Wyeomyia smithii

Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, Oregon 97403-5289, USA.
Genetics (Impact Factor: 5.96). 06/2007; 176(1):391-402. DOI: 10.1534/genetics.106.068726
Source: PubMed


A wide variety of temperate animals rely on length of day (photoperiodism) to anticipate and prepare for changing seasons by regulating the timing of development, reproduction, dormancy, and migration. Although the molecular basis of circadian rhythms regulating daily activities is well defined, the molecular basis for the photoperiodic regulation of seasonal activities is largely unknown. We use geographic variation in the photoperiodic control of diapause in the pitcher-plant mosquito Wyeomyia smithii to create the first QTL map of photoperiodism in any animal. For critical photoperiod (CPP), we detect QTL that are unique, a QTL that is sex linked, QTL that overlap with QTL for stage of diapause (SOD), and a QTL that interacts epistatically with the circadian rhythm gene, timeless. Results presented here confirm earlier studies concluding that CPP is under directional selection over the climatic gradient of North America and that the evolution of CPP is genetically correlated with SOD. Despite epistasis between timeless and a QTL for CPP, timeless is not located within any detectable QTL, indicating that it plays an ancillary role in the evolution of photoperiodism in W. smithii. Finally, we highlight one region of the genome that includes loci contributing to CPP, SOD, and hormonal regulation of development.

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Available from: Derrick K Mathias, Jul 29, 2014
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    • "polygenic, epistasis) or genomic architecture (e.g. chromosomal rearrangements), have confounded the identification of genes underlying variation in diapause timing (Tauber et al., 1977; Feder et al., 2002; Bradshaw et al., 2005; Mathias et al., 2007; Emerson et al., 2010; Wadsworth et al., 2015). Despite these difficulties, genes involved in the transitions of diapause phases have been identified. "
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    ABSTRACT: Rapid evolutionary change in seasonal timing can facilitate ecological speciation and resilience to climate warming. However, the molecular mechanisms behind shifts in animal seasonality are still unclear. Evolved differences in seasonality occur in the European corn borer moth (Ostrinia nubilalis), in which early summer emergence in E-strain adults and later summer emergence in Z-strain adults is explained by a shift in the length of the termination phase of larval diapause. Here, we sample from the developmental time course of diapause in both strains and use transcriptome sequencing to profile regulatory and amino acid changes associated with timing divergence. Within a previously defined QTL, we nominate 48 candidate genes including several in the insulin signaling and circadian rhythm pathways. Genome-wide transcriptional activity is negligible during the extended Z-strain termination, whereas shorter E-strain termination is characterized by a rapid burst of regulatory changes involved in resumption of the cell cycle, hormone production, and stress response. Although gene expression during diapause termination in Ostrinia is similar to that found previously in flies, nominated genes for shifts in timing are species-specific. Hence, across distant relatives the evolution of insect seasonality appears to involve unique genetic switches that direct organisms into distinct phases of the diapause pathway through wholesale restructuring of conserved gene regulatory networks.
    Journal of Experimental Biology 09/2015; 218(Pt 22). DOI:10.1242/jeb.126136 · 2.90 Impact Factor
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    • "Behavioural and physiological, especially endocrinological , changes associated with diapause development have been intensively studied in several species during the last 100 years (eg Tauber et al., 1986; de Kort, 1990; Denlinger, 2002). However, the genetic and molecular mechanisms underpinning diapause development are less well known (eg Mathias et al., 2007; MacRae, 2010; Ragland et al., 2011; Schmidt, 2011; Fabian et al., 2012). For instance, the underlying molecular machinery that senses photoperiodic changes and integrates and conveys this information to downstream endocrinological elements remains poorly understood (Sim & Denlinger, 2008). "
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    ABSTRACT: Behavioral and physiological changes during diapause, an important strategy of insects for surviving harsh seasonal conditions, have been intensively studied. The genetic and molecular mechanisms underpinning diapause development are less well known. We took a candidate gene approach to study pre-diapause gene expression patterns in the Colorado potato beetle (Leptinotarsa decemlineata), an invasive insect which has rapidly spread northwards to high seasonality environments. Newly eclosed beetles originating from southern (Italy) and northern (Russia) Europe were reared under short- (12L:12D) and long-day (18L:6D) photoperiods for 10 days. This time period includes the sensitive period for the photoperiodic induction and initiation of diapause. Gene expression trajectories of 12 diapause related genes (regulatory, metabolic and stress-resistance) were analyzed from 0, 5 and 10 day-old beetles. Gene expression differences increased with age, deviating significantly between populations and photoperiods in 10 day-old beetles. The gene expression profiles, particularly related to energy metabolism and stress-resistance, indicate that beetles originating from Russia prepare for diapause also under the long-day photoperiod and show qualitative differences in the diapausing phenotype. Our study shows that population dependent differences seen in behavioral and physiological traits connected with diapause in L. decemlineata are evident also in the expression trajectories of diapause-related genes.
    Insect Molecular Biology 07/2014; 23(5). DOI:10.1111/imb.12104 · 2.59 Impact Factor
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    • "However, most Drosophila studies focus on the ability to enter diapause as a binary response and do not address whether the identified loci are responsible for change in diapause timing and synchronization with seasonal environments. In contrast, the evolution of diapause timing has been emphasised in moths, butterflies , and pitcher plant mosquitoes, leading to clearly identified quantitative trait loci (QTL) (Dopman et al., 2005; Mathias et al., 2007; Kunte et al., 2011). Yet, the identity of the causal loci in these genomic regions and how allelic variation leads to altered physiological pathways and shifts in seasonal timing in nature all remain as outstanding questions. "
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    ABSTRACT: Evolutionary change in the timing of dormancy enables animals and plants to adapt to changing seasonal environments and can result in ecological speciation. Despite its clear biological importance, the mechanisms underlying the evolution of dormancy timing in animals remain poorly understood because of a lack of anatomical landmarks to discern which phase of dormancy an individual is experiencing. Taking advantage of the nearly universal characteristic of metabolic suppression during insect dormancy (diapause), we use patterns of respiratory metabolism to document physiological landmarks of dormancy and test which of the distinct phases of the dormancy developmental pathway contribute to a month-long shift in diapause timing between a pair of incipient moth species. Here, we show that divergence in life cycle between the earlier-emerging E-strain and the later-emerging Z-strain of European corn borer (ECB) is clearly explained by a delay in the timing of the developmental transition from the diapause maintenance phase to the termination phase. Along with recent findings indicating that life-cycle differences between ECB strains stem from allelic variation at a single sex-linked locus, our results demonstrate how dramatic shifts in animal seasonality can result from simple developmental and genetic changes. Although characterizing the multiple phases of the diapause developmental programme in other locally adapted populations and species will undoubtedly yield surprises about the nature of animal dormancy, results in the ECB moth suggest that focusing on genetic variation in the timing of the dormancy termination phase may help explain how (or whether) organisms rapidly respond to global climate change, expand their ranges after accidental or managed introductions, undergo seasonal adaptation, or evolve into distinct species through allochronic isolation.
    Journal of Evolutionary Biology 09/2013; 26(11). DOI:10.1111/jeb.12227 · 3.23 Impact Factor
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