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

Abstract

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.T HE annual change in day length at temperate latitudes provides a highly reliable indicator of future seasonal events and a wide variety of organisms use day length (photoperiod) to time their development, reproduction, dormancy, and migration. Concordance between individual photoperiodic response and local climate is an essential component of fitness for animals living in the temperate zone (Bradshaw et al. 2004), and modification of photoperiodic response is an important adaptation of animals during range expansion (Danilevskii 1965;Cooke 1977;Tauber et al. 1986;Danks 1987;Lounibos et al. 2003) or when confronted with rapid climate change (Bradshaw and Holzapfel 2001a, 2006). Photoperiodism provides an ecologically relevant, highly heritable trait whose adaptive significance in a temperate seasonal environment is not questioned. Length of the favorable or growing season in North America decreases with increasing latitude (Bradshaw 1976). Consequently, the optimal time to enter diapause advances to an earlier day in the year and the day length used to switch from active development to diapause [hereafter, the critical photoperiod (CPP)] is positively correlated with latitude and altitude among a wide variety of temperate arthropods (Danilevskii 1965;Taylor and Spalding 1986;Danks 1987). The consistent genetic change in photoperiodic response over geographic and climatic gradients provides one of the most robust examples of repeated adaptive evolution in nature.Although much progress has been made in identifying the genetic components of the circadian clock regulating daily activities, the molecular basis of the photoperiodic timer regulating seasonal activities is conspicuously absent from the ...

Footprints in time: comparative quantitative trait loci mapping of the pitcher-plant mosquito,Wyeomyia smithii

“…This result contrasts with our previous QTL analysis [23] that identified several epistatic interactions in an Alberta  Florida cross, using exactly the same analytical methodology. More strikingly, the lack of bi-marker epistasis in the ME  AL and AL  ME crosses contrasts with line crosses that consistently identify the effects of epistasis in genetic divergence of photoperiodic response between southern and northern populations [22,36,37] and despite the conservative nature of line-cross analysis that only detects net directional epistasis [39].…”

“…In the seventh hybrid generation, we phenotyped 1682 individuals in the NJ Â ME cross, 1886 individuals in the AL Â ME cross and 1176 individuals in the ME Â AL cross. We then chose for genotyping an equal number of males and females to minimize the effects of sex linkage [23] and chose individuals of both sexes spread evenly throughout the distribution of critical photoperiods to maximize discriminating power (see the electronic supplementary material, figure S1). …”

Genetic correlations and the evolution of photoperiodic time measurement within a local population of the pitcher-plant mosquito, Wyeomyia smithii

“…However, if one looks only for connections between circadian clock genes and photoperiodism, one is going to implicate only circadian clock genes to the exclusion of other possibilities. Others (Takahashi et al, 2008;Tauber and Kyriacou, 2008), as well as ourselves (Mathias et al, 2007;Emerson et al, 2009a, b;Bradshaw and Holzapfel, 2010a) have therefore urged application of circadianunbiased, forward-genetic approaches. If truly circadian-unbiased approaches identify circadian genes contributing to photoperiodic time measurement, then they do; however, using only circadian clock genes as candidate loci myopically ignores other possibilities, both conceptually and in the design of experiments and in the interpretation of their results.…”

“…The CPP mediating diapause is positively correlated with latitude and altitude of origin with R 2 repeatedly 492% (Bradshaw and Holzapfel, 2001). Photoperiodic response and rhythmic response to NH are polygenic traits involving additive, dominance and epistatic effects both within and between populations of W. smithii (Hard et al, 1993;Lair et al, 1997;Bradshaw et al, 2005;Mathias et al, 2006Mathias et al, , 2007. As CPP and amplitude of response to NH are quantitative traits, separating them is by definition quantitative in nature.…”

Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

“…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.…”