Natural Selection Favors a Newly Derived
            <i>timeless</i>
            Allele in
            <i>Drosophila melanogaster</i>

Tauber, Eran; Zordan, Mauro Agostino; Sandrelli, Federica; Pegoraro, Mirko; Osterwalder, Nicolò; Breda, Carlo; Daga, Andrea; Selmin, Alessandro; Monger, Karen; Benna, Clara; Rosato, Ezio; Kyriacou, Charalambos P.; Costa, Rodolfo

doi:10.1126/science.1138412

Cited by 289 publications

(382 citation statements)

References 21 publications

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“…Flies were raised at 25°C in LD12:12 cycles. Congenic male per s , per L , and per 01 mutants were backcrossed for six generations to a w 1118 that had itself been previously backcrossed for 10 generations to the wild HU strain, isolated from the Netherlands in 2005, and maintained as isofemale lines (30). As per maps very closely to w, we followed the per allele in each backcross generation by eye color and confirmed the final strains behaviorally in circadian locomotor assays.…”

Section: Methodsmentioning

confidence: 94%

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

Green

O’Callaghan²,

Hansen

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Under standard laboratory conditions of rectangular light/dark cycles and constant warm temperature, Drosophila melanogaster show bursts of morning (M) and evening (E) locomotor activity and a “siesta” in the middle of the day. These M and E components have been critical for developing the neuronal dual oscillator model in which clock gene expression in key cells generates the circadian phenotype. However, under natural European summer conditions of cycling temperature and light intensity, an additional prominent afternoon (A) component that replaces the siesta is observed. This component has been described as an “artifact” of the TriKinetics locomotor monitoring system that is used by many circadian laboratories world wide. Using video recordings, we show that the A component is not an artifact, neither in the glass tubes used in TriKinetics monitors nor in open-field arenas. By studying various mutants in the visual and peripheral and internal thermo-sensitive pathways, we reveal that the M component is predominantly dependent on visual input, whereas the A component requires the internal thermo-sensitive channel transient receptor potential A1 (TrpA1). Knockdown of TrpA1 in different neuronal groups reveals that the reported expression of TrpA1 in clock neurons is unlikely to be involved in generating the summer locomotor profile, suggesting that other TrpA1 neurons are responsible for the A component. Studies of circadian rhythms under seminatural conditions therefore provide additional insights into the molecular basis of circadian entrainment that would otherwise be lost under the usual standard laboratory protocols.

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Section: Methodsmentioning

confidence: 94%

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

Green

O’Callaghan²,

Hansen

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Diapause induction was also studied in association with allelic variation in the gene timeless (tim) (35), which encodes a light-responsive component of the circadian clock (36). As diapause expression is dependent on photoperiod, the authors hypothesized that this gene might impact reproductive diapause.…”

Section: Discussionmentioning

confidence: 99%

“…In particular, a newly derived allele, ls-tim, increases in frequency across Europe, raising a possible association between temperate habitats, diapause incidence, and tim allele frequencies. Tauber et al (36) showed that in three populations there was a significant relationship between the proportion expressing diapause, the testing photoperiod, and homozygous genotypes for the timeless alleles s-tim and ls-tim. It will be interesting to determine whether a similar association exists for the timeless alleles and diapause in North American populations, and in particular whether there is a latitudinal cline, as would be predicted.…”

Section: Discussionmentioning

confidence: 99%

An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster

Schmidt

Zhu

Das

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

186

219

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Diapause is the classic adaptation to seasonality in arthropods, and its expression can result in extreme lifespan extension as well as enhanced resistance to environmental challenges. Little is known about the underlying evolutionary genetic architecture of diapause in any organism. Drosophila melanogaster exhibits a reproductive diapause that is variable within and among populations; the incidence of diapause increases with more temperate climates and has significant pleiotropic effects on a number of life history traits. Using quantitative trait mapping, we identified the RNAbinding protein encoding gene couch potato (cpo) as a major genetic locus determining diapause phenotype in D. melanogaster and independently confirmed this ability to impact diapause expression through genetic complementation mapping. By sequencing this gene in samples from natural populations we demonstrated through linkage association that variation for the diapause phenotype is caused by a single Lys/Ile substitution in one of the six cpo transcripts. Complementation analyses confirmed that the identified amino acid variants are functionally distinct with respect to diapause expression, and the polymorphism also shows geographic variation that closely mirrors the known latitudinal cline in diapause incidence. Our results suggest that a naturally occurring amino acid polymorphism results in the variable expression of a diapause syndrome that is associated with the seasonal persistence of this model organism in temperate habitats.cline ͉ diapause ͉ life history ͉ mapping ͉ tradeoff N atural populations encounter environmental stresses that diminish individual fitness, and these stresses are variable across space and time. It is predicted that the resulting natural selection often leads to a situation in which no genotype has the highest fitness across all environments, and polymorphism is maintained. This concept is pervasive in arguments about the evolution of life history variation and associated genetic tradeoffs (1). However, the expected molecular polymorphism associated with life history tradeoffs and adaptation remains elusive. Although we would expect these phenomena to be universal, the complexities of genetic dissection of such variation suggest that the best opportunity to identify the genetic basis for life history variation lies in the study of the genetic models in their natural populations (2).Drosophila melanogaster is a human commensal that has spread from areas of Sub-Saharan Africa to Europe and Asia, possibly over the last 5,000 to 16,000 years, and into the Western Hemisphere and Australia in the past several hundred years (3-5). This worldwide expansion from the tropics has required adaptation to the pronounced seasonality present in temperate habitats, and there are many examples of both single-gene polymorphism and quantitative trait variation that show geographic patterns associated with the transition from tropical to temperate climates in this species (6, 7). There also is good evidence that D. melanogaster ov...

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“…43 -46 Moreover, a latitudinally structured length polymorphism at the timeless clock gene of D. melanogaster has been recently implicated in the photoperiod-and temperature-dependent adaptive life-history trait of diapause. 47,48 The finding of latitudinally structured clock gene polymorphisms exclusively in poikilotherms might suggest that thermal selection more than latitudinal changes in day length would have played the major role in such polymorphisms (but see Sandrelli et al 47 and Tauber et al 48 ). However, a latitudinal cline for a length polymorphism in the Clock gene of a homeothermal avian species, the nonmigratory passerine Cyanistes caeruleus, has been recently described, suggesting that, at least in this case, an additional significant role for other environmental parameters, that is photoperiodicity, could be important.…”

Section: Discussionmentioning

confidence: 99%

Genetic diversity patterns at the human clock gene period 2 are suggestive of population-specific positive selection

et al. 2008

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Period 2 (PER2) is a key component of the mammalian circadian clock machinery. In humans, genetic variation of clock genes or chronic disturbance of circadian rhythmicity has been implied in the onset of several phenotypes, ranging from periodic insomnias to advanced or delayed sleep phases, to more severe disorders. Peculiar geographic diversity patterns in circadian genes might represent an adaptive response to different light/dark cycles or environmental changes to which different human populations are exposed. To investigate the degree and nature of PER2 gene variation in human populations of different geographic origin, and its possible correlation with different latitudes, we sequenced a 7.7 kb portion of the gene in 20 individuals worldwide. In total, 25 variable sites were identified. The geographic distribution of haplotypes defined by five polymorphic sites was analyzed in 499 individuals from 11 populations from four continents. No evidence for latitude-driven selective effects on PER2 genetic variability was found. However, a high and significant difference in the geographic distribution of PER2 polymorphisms was observed between Africans and non-Africans, suggesting a history of geographically restricted natural selection at this locus. In support of this notion, we found several signals for selection in the sequences. The putative selected haplotype showed a recent coalescent age (8.7 Kyr), and an unusually high frequency in non-African populations. Overall, these findings indicate that a human clock-relevant gene, PER2, might have been influenced by positive selection, and offer preliminary insights into the evolution of this functional class of genes.

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Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster

Cited by 289 publications

References 21 publications

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster

Genetic diversity patterns at the human clock gene period 2 are suggestive of population-specific positive selection

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