Evidence that natural selection maintains genetic variation for sleep in Drosophila melanogaster

BMC Evolutionary Biology

David J Begun²  Joanna C Chiu¹  Perot Saelao²  Li Zhao²  Nicolas Svetec² 

[1] Department of Entomology and Nematology, University of California, Davis, CA, USA;Department of Evolution and Ecology, University of California, 3352 Storer Hall, One Shields Ave., Davis 95616, CA, USA

关键词: RNA-seq;    Gene expression;    Circadian rhythms;    Sleep;    Locomotor activity;    Spatially varying selection;    Latitudinal cline;    Drosophila melanogaster;   

Others  :  1158278
DOI  :  10.1186/s12862-015-0316-2

 received in 2014-11-21, accepted in 2015-02-24,  发布年份 2015

【 摘 要 】

Background

Drosophila melanogaster often shows correlations between latitude and phenotypic or genetic variation on different continents, which suggests local adaptation with respect to a heterogeneous environment. Previous phenotypic analyses of latitudinal clines have investigated mainly physiological, morphological, or life-history traits. Here, we studied latitudinal variation in sleep in D. melanogaster populations from North and Central America. In parallel, we used RNA-seq to identify interpopulation gene expression differences.

Results

We found that in D. melanogaster the average nighttime sleep bout duration exhibits a latitudinal cline such that sleep bouts of equatorial populations are roughly twice as long as those of temperate populations. Interestingly, this pattern of latitudinal variation is not observed for any daytime measure of activity or sleep. We also found evidence for geographic variation for sunrise anticipation. Our RNA-seq experiment carried out on heads from a low and high latitude population identified a large number of gene expression differences, most of which were time dependent. Differentially expressed genes were enriched in circadian regulated genes and enriched in genes potentially under spatially varying selection.

Conclusion

Our results are consistent with a mechanistic and selective decoupling of nighttime and daytime activity. Furthermore, the present study suggests that natural selection plays a major role in generating transcriptomic variation associated with circadian behaviors. Finally, we identified genomic variants plausibly causally associated with the observed behavioral and transcriptomic variation.

【 授权许可】

   
2015 Svetec et al.; licensee BioMed Central

【 图 表 】

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【 参考文献 】

• [1]Hedrick PW: Genetic polymorphism in heterogeneous environments: the Age of genomics. Annu Rev Ecol Evol Syst 2006, 37:67-93.
• [2]Mitchell-Olds T, Willis JH, Goldstein DB: Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 2007, 8:845-56.
• [3]De Jong G, Bochdanovits Z: Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. J Genet 2003, 82:207-23.
• [4]Hut RA, Beersma DGM: Evolution of time-keeping mechanisms: early emergence and adaptation to photoperiod. Philos Trans R Soc Lond B Biol Sci 2011, 366:2141-54.
• [5]Shaw PJ: Correlates of sleep and waking in Drosophila melanogaster. Science (80- ) 2000, 287:1834-7.
• [6]Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, et al.: Rest in Drosophila is a sleep-like state. Neuron 2000, 25:129-38.
• [7]Nitz DA, Van SB, Tononi G, Greenspan RJ, Jay J, Drive H, et al.: Electrophysiological Correlates of Rest and Activity in Drosophila melanogaster. Curr Biol 2002, 12:1934-40.
• [8]Van Alphen B, Yap MHW, Kirszenblat L, Kottler B, van Swinderen B: A dynamic deep sleep stage in Drosophila. J Neurosci 2013, 33:6917-27.
• [9]Koh K, Evans JM, Hendricks JC, Sehgal A: A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci U S A 2006, 103:13843-7.
• [10]Seugnet L, Suzuki Y, Donlea JM, Gottschalk L, Shaw PJ: Sleep deprivation during early-adult development results in long-lasting learning deficits in adult Drosophila. Sleep 2011, 34:137-46.
• [11]Li X, Yu F, Guo A: Sleep deprivation specifically impairs short-term olfactory memory in Drosophila. Sleep 2009, 32:1417-24.
• [12]Barnard AR, Nolan PM: When clocks go bad: neurobehavioural consequences of disrupted circadian timing. PLoS Genet 2008, 4:e1000040.
• [13]Shaw PJ, Tononi G, Greenspan RJ, Robinson DF: Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 2002, 417:287-91.
• [14]Harbison ST, McCoy LJ, Mackay TFC: Genome-wide association study of sleep in Drosophila melanogaster. BMC Genomics 2013, 14:281.
• [15]Nall AH, Sehgal A: Small-molecule screen in adult Drosophila identifies VMAT as a regulator of sleep. J Neurosci 2013, 33:8534-40.
• [16]Freeman AAH, Syed S, Sanyal S: Modeling the genetic basis for human sleep disorders in Drosophila. Commun Integr Biol 2013, 6:e22733.
• [17]Picot M, Cusumano P, Klarsfeld A, Ueda R, Rouyer F: Light activates output from evening neurons and inhibits output from morning neurons in the Drosophila circadian clock. PLoS Biol 2007, 5:e315.
• [18]Ishimoto H, Lark A, Kitamoto T: Factors that differentially affect daytime and nighttime sleep in Drosophila melanogaster. Front Neurol 2012, 3:24.
• [19]Grima B, Chélot E, Xia R, Rouyer F: Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 2004, 431:869-73.
• [20]Stoleru D, Peng Y, Rosbash M: Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 2004, 431:862-8.
• [21]Vanin S, Bhutani S, Montelli S, Menegazzi P, Green EW, Pegoraro M, et al.: Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 2012, 484:371-5.
• [22]Majercak J, Sidote D, Hardin PE, Edery I: How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 1999, 24:219-30.
• [23]Rodriguez J, Tang C-HA, Khodor YL, Vodala S, Menet JS, Rosbash M: Nascent-Seq analysis of Drosophila cycling gene expression. Proc Natl Acad Sci U S A 2013, 110:E275-84.
• [24]Hughes ME, Grant GR, Paquin C, Qian J, Nitabach MN: Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res 2012, 22:1266-81.
• [25]Boothroyd CE, Wijnen H, Naef F, Saez L, Young MW: Integration of light and temperature in the regulation of circadian gene expression in Drosophila. PLoS Genet 2007, 3:e54.
• [26]Abruzzi KC, Rodriguez J, Menet JS, Desrochers J, Zadina A, Luo W, et al.: Drosophila CLOCK target gene characterization: Implications for circadian tissue-specific gene expression. Genes Dev 2011, 25:2374-86.
• [27]Cirelli C, LaVaute TM, Tononi G: Sleep and wakefulness modulate gene expression in Drosophila. J Neurochem 2005, 94:1411-9.
• [28]Massouras A, Waszak SM, Albarca-Aguilera M, Hens K, Holcombe W, Ayroles JF, et al.: Genomic variation and its impact on gene expression in Drosophila melanogaster. PLoS Genet 2012, 8:e1003055.
• [29]Holsinger KE, Weir BS: Genetics in geographically structured populations: defining, estimating and interpreting F(ST). Nat Rev Genet 2009, 10:639-50.
• [30]Kolaczkowski B, Kern AD, Holloway AK, Begun DJ: Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 2011, 187:245-60.
• [31]Reinhardt JA, Kolaczkowski B, Jones CD, Begun DJ, Kern AD: Parallel geographic variation in Drosophila melanogaster. Genetics 2014, 197:361-73.
• [32]Zhang Y, Ling J, Yuan C, Dubruille R, Emery P: A role for Drosophila ATX2 in activation of PER translation and circadian behavior. Science 2013, 340:879-82.
• [33]Lim C, Allada R: ATAXIN-2 activates PERIOD translation to sustain circadian rhythms in Drosophila. Science 2013, 340:875-9.
• [34]Lear BC, Darrah EJ, Aldrich BT, Gebre S, Scott RL, Nash HA, et al.: UNC79 and UNC80, putative auxiliary subunits of the NARROW ABDOMEN ion channel, are indispensable for robust circadian locomotor rhythms in Drosophila. PLoS One 2013, 8:e78147.
• [35]Livingstone MS, Tempel BL: Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 1983, 303:67-70.
• [36]Van Swinderen B, Andretic R: Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc R Soc B 2011, 278:906-13.
• [37]Carhan A, Tang K, Shirras CA, Shirras AD, Isaac RE: Loss of Angiotensin-converting enzyme-related (ACER) peptidase disrupts night-time sleep in adult Drosophila melanogaster. J Exp Biol 2011, 214(Pt 4):680-6.
• [38]Benito J, Hoxha V, Lama C, Lazareva AA, Ferveur J-F, Hardin PE, et al.: The circadian output gene takeout is regulated by Pdp1epsilon. Proc Natl Acad Sci U S A 2010, 107:2544-9.
• [39]Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlötterer C, et al.: Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol 2012, 21:4748-69.
• [40]Helfrich-Förster C: Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster–sex-specific differences suggest a different quality of activity. J Biol Rhythms 2000, 15:135-54.
• [41]Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al.: The developmental transcriptome of Drosophila melanogaster. Nature 2011, 471:473-9.
• [42]Tauber E, Zordan M, Sandrelli F, Pegoraro M, Osterwalder N, Breda C, et al.: Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 2007, 316:1895-8.
• [43]Currie J, Goda T, Wijnen H: Selective entrainment of the Drosophila circadian clock to daily gradients in environmental temperature. BMC Biol 2009, 7:49.
• [44]Sandrelli F, Tauber E, Pegoraro M, Mazzotta G, Cisotto P, Landskron J, et al.: A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 2007, 316:1898-900.
• [45]Harbison ST, Carbone MA, Ayroles JF, Stone EA, Lyman RF, Mackay TFC: Co-regulated transcriptional networks contribute to natural genetic variation in Drosophila sleep. Nat Genet 2009, 41:371-5.
• [46]Chiu JC, Low KH, Pike DH, Yildirim E, Edery I: Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J Vis Exp 2010, 43:e2157.
• [47]Klarsfeld A, Leloup J-C, Rouyer F: Circadian rhythms of locomotor activity in Drosophila. Behav Processes 2003, 64:161-75.
• [48]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-11.
• [49]Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-2.
• [50]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
• [51]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al.: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:516-20.