Accuracy of fruit-fly eclosion rhythms evolves by strengthening circadian gating rather than developmental fine-tuning

Abstract

Fruit flies (Drosophila melanogaster) eclose from their pupae mainly around dawn. The timing of eclosion is thought to confer adaptive benefits to the organisms and thus shows remarkable accuracy. However, it is not clear what factors are involved in the evolution of such accuracy in natural populations. In this study, we examined the relative contributions of gating of eclosion by the circadian clock versus clock-independent developmental rates and light-induced responses in the eclosion phenotype exhibited by fly populations that have evolved greater accuracy in eclosion rhythms compared to controls. We compared variation in timing of transitions between early developmental stages (pupariation and pigmentation), overall development time under constant light conditions – where circadian clocks are dysfunctional – and eclosion profiles when developmental rate was manipulated using different larval densities in selected and control stocks. Our results showed that stocks that have evolved greater accuracy of eclosion rhythms due to artificial selection do not show reduced individual variation in pupariation and pigmentation time compared to controls, though they do exhibit lower variation in eclosion time. Selected stocks also did not show lower variation in eclosion time under constant light conditions in contrast to the greater accuracy seen under light-dark cycles. Moreover, manipulations of developmental rate by varying larval density and inducing eclosion by changing onset of light phase did not alter the eclosion profile of selected stocks as much as it did controls, since selected stocks largely restricted eclosion to the daytime. These results suggest that fly populations selected for greater accuracy have evolved accurate eclosion rhythms primarily by strengthening circadian gating of eclosion rather than due to fine-tuning of clock-independent developmental processes.

The clock gene Cryptochrome 1 is involved in the photoresponse of embryonic hatching behavior in Bombyx mori

“…Similar to adult emergence, embryo hatching is also considered to be a “gating” process (Mark et al, 2021; Varma et al, 2019; Villamizar et al, 2013). The role of the clock is defined as a gated switch, by which the clock imposes a daily rhythm on the embryo/adult during the gated period, initiating the hatching/emergence process (Myers, 2003; Qiu & Hardin, 1996).…”

Natural alleles of the clock gene timeless differentially affect life-history traits in Drosophila

“…On the other hand, it is worth highlighting that these data refer to pupariation time, and not eclosion. Thus, it is still possible that both s-tim and ls-tim homozygous flies maintain a circadian rhythm in eclosion, differentially regulating the timing of the final steps of metamorphosis and/or circadian gating of eclosion ( Varma et al, 2019 ; Mark et al, 2021 ). Further, we hypothesize that the identified delay might be instrumental to prolong larval feeding and thus the growth phase, resulting in larger flies, a trait which is strongly selected at higher latitudes ( Chown and Gaston, 2010 ; Stillwell, 2010 ), and is a feature of diapause-destined individuals in several insect species ( Hahn and Denlinger, 2011 ).…”

Drosophila Tet Is Required for Maintaining Glial Homeostasis in Developing and Adult Fly Brains

“…In particular, dTet has been shown to be required during embryonic and larval stages in PDF neurons to ensure proper circadian behavior in adult flies ( Wang et al, 2018 ). In fact, the circadian rhythm also modulates the timing of preadult developmental events in Drosophila ( Yadav et al, 2014 ; Varma et al, 2019 ) and thus, defects in the circadian clock might contribute to the observed lethality.…”