Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster

Department of Genetics, University of Leicester, Leicester LE1 7RH, UK.
Science (Impact Factor: 33.61). 07/2007; 316(5833):1895-8. DOI: 10.1126/science.1138412
Source: PubMed


Circadian and other natural clock-like endogenous rhythms may have evolved to anticipate regular temporal changes in the environment. We report that a mutation in the circadian clock gene timeless in Drosophila melanogaster has arisen and spread by natural selection relatively recently in Europe. We found that, when introduced into different genetic backgrounds, natural and artificial alleles of the timeless gene affect the incidence of diapause in response to changes in light and temperature. The natural mutant allele alters an important life history trait that may enhance the fly's adaptation to seasonal conditions.

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    • "In the fruit fly particularly, a number of novel features have been revealed in seminatural conditions, which require some revisions of our current understanding of how the clock responds to natural entraining stimuli (Vanin et al., 2012). Natural polymorphic variants of period (per) and timeless (tim) have been described that appear to be under selection and adapt fruit flies to various thermal and photoperiodic seasonal environments (Rosato et al., 1997; Sawyer et al., 1997, 2006; Sandrelli et al., 2007; Tauber et al., 2007). However a more dynamic flexibility to respond to daily or seasonal changes in temperature has been observed in per splicing patterns , where a thermosensitive alternative splicing of an 89-bp intron in the 3′ UTR yields per spliced as opposed to the per unspliced form generated at higher temperatures (Majercak et al., 1999, 2004; Collins et al., 2004; Low et al., 2012). "
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    ABSTRACT: Previous analysis of Drosophila circadian behavior under natural conditions has revealed a number of novel and unexpected features. Here we focus on the oscillations of per and tim mRNAs and their posttranscriptional regulation and observe significant differences in molecular cycling under laboratory and natural conditions. In particular, robust per mRNA cycling from fly heads is limited to the summers, whereas tim RNA cycling is observed throughout the year. When both transcripts do cycle, their phases are similar, except for the very warmest summer months. We also study the natural splicing profiles of per and tim transcripts and observe a clear relationship between temperature and splicing. In natural conditions, we confirm the relationship between accumulation of the per(spliced) variant, low temperature, and the onset of the evening component of locomotor activity, first described in laboratory conditions. Intriguingly, in the case of tim splicing, we detect the opposite relationship, with tim(spliced) expression increasing at higher temperatures. A first characterization of the 4 different TIM protein isoforms (resulting from the combination of the natural N-terminus length polymorphism and the C-terminus alternative splicing) using the 2-hybrid assay showed that the TIM(unspliced) isoforms have a stronger affinity for CRY, but not for PER, suggesting that the tim 3' splicing could have physiological significance, possibly in temperature entrainment and/or adaptation to seasonal environments. © 2015 The Author(s).
    Journal of Biological Rhythms 06/2015; 30(3):217-27. DOI:10.1177/0748730415583575 · 2.77 Impact Factor
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    • "Light sensitivity of the circadian clock is known to be influenced by a naturally occurring polymorphism in the timeless (tim) gene (Sandrelli et al., 2007; Tauber et al., 2007). To exclude possible effects of this tim polymorphism, we crossed all photoreceptor mutants into the ls-tim background (Schlichting et al., 2014) and used the wild-type strain WT CantonS with the same ls-tim background as control. "
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    ABSTRACT: Light is the most important zeitgeber for the synchronization of the Drosophila melanogaster circadian clock. In nature, there is twilight, and the nights are rarely completely dark, a fact that is usually disregarded in lab experiments. Recent studies showed contrary effects of simulated twilight and moonlight on fly locomotor activity, with twilight shifting morning and evening activity into the day and moonlight shifting it into the night. A currently unanswered question is, what may happen to locomotor activity when flies are exposed to more natural conditions in which both moonlight and twilight are simulated? Our data demonstrate that flies are able to integrate twilight and moonlight. However, twilight seems to dominate over moonlight as both, morning and evening activity peaks, take place at dawn or at dusk, respectively, and not during the night. Furthermore, nocturnal activity decreases in the presence of twilight. The compound eyes are essential for this behavior, and by investigating different photoreceptor mutants, we unraveled the importance of photoreceptor cells 7 and 8 for wild-type phases of the activity peaks. To adjust nocturnal activity levels to a wild-type manner, all photoreceptor cells work together in a complex way, with rhodopsin 6 having a prominent role. © 2015 The Author(s).
    Journal of Biological Rhythms 04/2015; 30(2):117-28. DOI:10.1177/0748730415575245 · 2.77 Impact Factor
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    • "Rather than being physically linked in ECB, cry1 and period could show correlations as a consequence of epistatic selection, possibly because of their interactions with timeless, a gene showing clinal variation in Drosophila (Tauber et al., 2007). It is unclear why multiple circadian genes show correlated changes associated with voltinism in ECB and which gene(s) in the pathway might be the primary target(s) of natural selection. "
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    ABSTRACT: Many temperate insects take advantage of longer growing seasons at lower latitudes by increasing their generation number or voltinism. In some insects, development time abruptly decreases when additional generations are fit into the season. Consequently, latitudinal "sawtooth" clines associated with shifts in voltinism are seen for phenotypes correlated with development time, like body size. However, latitudinal variation in voltinism has not been linked to genetic variation at specific loci. Here we show a pattern in allele frequency among voltinism ecotypes of the European corn borer moth (Ostrinia nubilalis) that is reminiscent of a sawtooth cline. We characterized 145 autosomal and sex-linked SNPs and found that period, a circadian gene that is genetically linked to a major QTL determining variation in post-diapause development time, shows cyclical variation between voltinism ecotypes. Allele frequencies at an unlinked circadian clock gene cryptochrome1 were correlated with period. These results suggest that selection on development time to 'fit' complete life cycles into a latitudinally varying growing season produce oscillations in alleles associated with voltinism, primarily through changes at loci underlying the duration of transitions between diapause and other life history phases. Correlations among clock loci suggest possible coupling between the circadian clock and the circannual rhythms for synchronizing seasonal life history. We anticipate that latitudinal oscillations in allele frequency will represent signatures of adaptation to seasonal environments in other insects and may be critical to understanding the ecological and evolutionary consequences of variable environments, including response to global climate change. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Journal of Evolutionary Biology 11/2014; 28(1). DOI:10.1111/jeb.12562 · 3.23 Impact Factor
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