Diapause in Drosophila melanogaster – Photoperiodicity, cold tolerance and metabolites

Anduaga, Ane Martín; Nagy, Dóra; Costa, Rodolfo; Kyriacou, Charalambos P.

doi:10.1016/j.jinsphys.2018.01.003

Cited by 51 publications

(36 citation statements)

References 27 publications

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“…This provides a suitable readout to investigate the effect of eya genetic manipulation in the photoperiodic control of seasonal physiology. As shown in previous studies (18), we found that temperature above 10-12°C was not sufficient to induce D. melanogaster reproductive dormancy in SP.…”

Section: Resultssupporting

confidence: 67%

“…Whether D. melanogaster represents a suitable model to study diapause has been under debate. However recent studies suggest that the photoperiodic component of D. melanogaster might be more robust than previously described (18, 19). We found that newly emerged females reared at 10°C for 28 days, exhibit significantly smaller ovaries when exposed to short photoperiod (SP 8L:16D) compared to long photoperiod (LP 16L:8D).…”

Section: Introductionmentioning

confidence: 76%

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EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

Abrieux

Xue

Cai

et al. 2020

Preprint

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Organisms possess photoperiodic timing mechanisms to anticipate variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that in Drosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation of eya expression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in female D. melanogaster. Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations that tim null mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressing tim show an increased incidence of reproductive dormancy even in long photoperiod.Significance StatementExtracting information on calendar time from seasonal changes in photoperiod and temperature is critical for organisms to maintain circannual cycles in physiology and behavior. Here we found that in flies, EYES ABSENT (EYA) protein act as a seasonal sensor by adjusting its abundance and circadian phase in response to changes in photoperiod and temperature. We show that the manipulation of EYA levels is sufficient to impair the ability of female Drosophila to regulate seasonal variation in reproductive dormancy. Finally, our results suggest an important role of the circadian clock protein TIMELESS (TIM) in modulating EYA level through its ability to measure night length, linking the circadian clock to seasonal timing.

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Section: Resultssupporting

confidence: 67%

Section: Introductionmentioning

confidence: 76%

EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

Abrieux

Xue

Cai

et al. 2020

Preprint

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“…Like other studies [24,35,36,94], we identify temperature and nutritional exposure as two critical variables that influence diapause and extend this analysis to outbred lab and field-caught samples. Specifically, we find that diapause induction is exquisitely sensitive to extremely small differences in temperature (Fig 2), emphasizing the importance of precise thermal control and monitoring for experiments studying diapause in this species [95]. This fine-grained sensitivity suggests that even temperature variation across shelves of an incubator or at different distances from a light source could potentially influence experimental outcomes; these potential sources of thermal variation were controlled in our experiment by our use of multiple environmental chambers with nearly identical physical setup aside from temperature and photoperiod.…”

Section: Discussionmentioning

confidence: 99%

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Erickson

Weller

Song

et al. 2020

Preprint

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Organisms living in seasonally variable environments utilize cues such as light and temperature to induce plastic responses, enabling them to exploit favorable seasons and avoid unfavorable ones. Local adapation can result in variation in seasonal responses, but the genetic basis and evolutionary history of this variation remains elusive. Many insects, including Drosophila melanogaster, are able to undergo an arrest of reproductive development (diapause) in response to unfavorable conditions. In D. melanogaster, the ability to diapause is more common in high latitude populations, where flies endure harsher winters, and in the spring, reflecting differential survivorship of overwintering populations. Using a novel hybrid swarm-based genome wide association study, we examined the genetic basis and evolutionary history of ovarian diapause. We exposed outbred females to different temperatures and day lengths, characterized ovarian development for over 2800 flies, and reconstructed their complete, phased genomes. We found that diapause, scored at two different developmental cutoffs, has modest heritability, and we identified hundreds of SNPs associated with each of the two phenotypes. Alleles associated with one of the diapause phenotypes tend to be more common at higher latitudes, but these alleles do not show predictable seasonal variation. The collective signal of many small-effect, clinally varying SNPs can plausibly explain latitudinal variation in diapause seen in North America. Alleles associated with diapause are segregating at relatively high frequencies in Zambia, suggesting that variation in diapause relies on ancestral polymorphisms, and both pro- and anti-diapause alleles have experienced selection in North America. Finally, we utilized outdoor mesocosms to track diapause under natural conditions. We found that hybrid swarms reared outdoors evolved increased propensity for diapause in late fall, whereas indoor control populations experienced no such change. Our results indicate that diapause is a complex, quantitative trait with different evolutionary patterns across time and space.Author SummaryAnimals exhibit diverse strategies to cope with unfavorable conditions in temperate, seasonally varying environments. The model fly, Drosophila melanogaster, can enter a physiological state known as diapause under winter-like conditions. Diapause is characterized by an absence of egg maturation in females and is thought to conserve energy for survival during stressful times. The ability to diapause is more common in flies from higher latitudes and in offspring from flies that have recently overwintered. Therefore, diapause has been thought to be a recent adaptation to temperate climates. We identified hundreds of genetic variants that affect diapause and found that some vary predictably across latitudes in North America. We found little signal of repeated seasonality in diapause-associated genetic variants, but our populations evolved an increased ability to diapause in the winter when they were exposed to natural conditions. Combined, our results suggest that diapause-associated variants evolve differently across space and time. We find little evidence that diapause evolved recently in temperate environments; rather, SNPs associated with diapause tend to be quite common in Zambia, suggesting that diapause may promote survival under stresses other than cold. Our results provide future targets for research into the genetic underpinnings of this complex, ecologically relevant trait.

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“…The molecular details of this photoperiodic timer are still elusive, despite decades of intense research (Bradshaw & Holzapfel 2010;Saunders et al 2004). Recently, however, significant progress has been made (Ojima et al 2018;Andreatta et al 2018;Anduaga et al 2018;Liao et al 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The response is manifested as an arrest of ovarian maturation in a pre-vitellogenic state that is characteristic of a reproductive diapause. The photoperiodic response in D. melanogaster is rather shallow, strain-specific and is largely masked by the temperature cycles (Anduaga et al 2018). A recent study suggested that the photoperiodic response of flies in the laboratory could be greatly enhanced by adopting a semi-natural lighting regime, as opposed to the rectangular light-dark cycles which is commonly used.…”

Section: Introductionmentioning

confidence: 99%

Photoperiod-dependent expression of MicroRNA in Drosophila

Pegoraro

Tauber

2018

Preprint

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Like many other insects in temperate regions, Drosophila melanogaster exploits the photoperiod shortening that occurs during the autumn as an important cue to trigger a seasonal response. Flies survives the winter by entering a state of reproductive arrest (diapause), which drives relocation of resources from reproduction to survival. Here, we profiled the expression of microRNA (miRNA) in long and short photoperiods, and identified seven differentially expressed miRNAs (dme-mir-2b, dme-mir-11, dme-mir-34, dme-mir-274, dme-mir-184, dme-mir-184* and dme-mir-285). Misexpression of dme-mir-2b, dmemir-184 and dme-mir-274 in pigment-dispersing factor-expressing neurons largely disrupted the normal photoperiodic response, suggesting that these miRNAs play functional roles in photoperiodic timing. We also analyzed the targets of photoperiodic miRNA by both computational predication and by Argonaute-1mediated immunoprecipitation of long-and short-day RNA samples. Together with global transcriptome profiling, our results expand existing data on other Drosophila species, identifying genes and pathways that are differentially regulated in different photoperiods and reproductive status. Our data suggest that post-transcriptional regulation by miRNA is an important facet of photoperiodic timing.

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Diapause in Drosophila melanogaster – Photoperiodicity, cold tolerance and metabolites

Cited by 51 publications

References 27 publications

EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Photoperiod-dependent expression of MicroRNA in Drosophila

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