Abstract
Nearly all organisms evolved endogenous self-sustained timekeeping mechanisms to track and anticipate cyclic changes in the environment. Circadian clocks, with a periodicity of about 24 h, allow animals to adapt to day-night cycles. Biological clocks are highly adaptive, but strong behavioral rhythms might be a disadvantage for adaptation to weakly rhythmic environments such as polar areas [1, 2]. Several high-latitude species, including Drosophila species, were found to be highly arrhythmic under constant conditions [3-6]. Furthermore, Drosophila species from subarctic regions can extend evening activity until dusk under long days. These traits depend on the clock network neurochemistry, and we previously proposed that high-latitude Drosophila species evolved specific clock adaptations to colonize polar regions [5, 7, 8]. We broadened our analysis to 3 species of the Chymomyza genus, which diverged circa 5 million years before the Drosophila radiation [9] and colonized both low and high latitudes [10,11]. C.costata, pararufithorax, and procnemis, independently of their latitude of origin, possess the clock neuronal network of low-latitude Drosophila species, and their locomotor activity does not track dusk under long photoperiods. Nevertheless, the high-latitude C.costata becomes arrhythmic under constant darkness (DD), whereas the two low-latitude species remain rhythmic. Different mechanisms are behind the arrhythmicity in DD of C.costata and the high-latitude Drosophila ezoana, suggesting that the ability to maintain behavioral rhythms has been lost more than once during drosophilids' evolution and that it might indeed be an evolutionary adaptation for life at high latitudes.
Highlights
One lateral neurons (LNs), located in close proximity to the s- and l-LNvs but intermediate in size between them (Figure S1A), is CRY positive but PDF negative and hereafter named PDFÀLNvs (Figures 1I–1K). We propose that this neuron corresponds to the 5th s-LNv of D. melanogaster [17]
Based on CRY and PDF functions in D. melanogaster [5, 25,26,27], we proposed that the loss of PDF in the s-LNvs and CRY in the l-LNvs in the high-latitude species might allow them to better cope with the long days typical of polar summers [5, 7, 8]
To verify whether C. costata shows a high-latitude behavior despite carrying a low-latitude clock network, we recorded its locomotor activity, as well as that of C. pararufithorax and C. procnemis, under light:dark (LD) cycles with 12, 16, and 20 h of light per day (LD12:12, LD16:8, and LD20:4, respectively; Figures 2 and S1)
Summary
Bertolini et al find that drosophilids inhabiting high latitudes possess a circadian clock that is either not selfsustained or uncoupled from its output. This leads to behavioral arrhythmicity in constant darkness. The authors propose that this feature might be of adaptive value for animals to successfully colonize weakly rhythmic environments. Highlights d The Chymomyza genus carries the ancestral low-latitude D. melanogaster-like clock d C. costata colonized high latitudes despite a low-latitude clock neuroarchitecture d High-latitude drosophilids show arrhythmicity in constant darkness d C. costata and D. ezoana achieve arrhythmicity via different strategies. 2019, Current Biology 29, 3928–3936 November 18, 2019 a 2019 The Author(s).
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