Timing the tides: Genetic control of diurnal and lunar emergence times is correlated in the marine midge Clunio marinus

Tobias S Kaiser,Dietrich Neumann,David G Heckel

doi:10.1186/1471-2156-12-49

Tobias S Kaiser, Dietrich Neumann + Show 1 more

Open Access

https://doi.org/10.1186/1471-2156-12-49

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Abstract

BackgroundThe intertidal zone of seacoasts, being affected by the superimposed tidal, diurnal and lunar cycles, is temporally the most complex environment on earth. Many marine organisms exhibit lunar rhythms in reproductive behaviour and some show experimental evidence of endogenous control by a circalunar clock, the molecular and genetic basis of which is unexplored. We examined the genetic control of lunar and diurnal rhythmicity in the marine midge Clunio marinus (Chironomidae, Diptera), a species for which the correct timing of adult emergence is critical in natural populations.ResultsWe crossed two strains of Clunio marinus that differ in the timing of the diurnal and lunar rhythms of emergence. The phenotype distribution of the segregating backcross progeny indicates polygenic control of the lunar emergence rhythm. Diurnal timing of emergence is also under genetic control, and is influenced by two unlinked genes with major effects. Furthermore, the lunar and diurnal timing of emergence is correlated in the backcross generation. We show that both the lunar emergence time and its correlation to the diurnal emergence time are adaptive for the species in its natural environment.ConclusionsThe correlation implies that the unlinked genes affecting lunar timing and the two unlinked genes affecting diurnal timing could be the same, providing an unexpectedly close interaction of the two clocks. Alternatively, the genes could be genetically linked in a two-by-two fashion, suggesting that evolution has shaped the genetic architecture to stabilize adaptive combinations of lunar and diurnal emergence times by tightening linkage. Our results, the first on genetic control of lunar rhythms, offer a new perspective to explore their molecular clockwork.

Highlights

The intertidal zone of seacoasts, being affected by the superimposed tidal, diurnal and lunar cycles, is temporally the most complex environment on earth
Certain tidal conditions re-occur predictably during the lunar cycle and the adaptive value of lunar rhythms can likely be attributed to restricting the delicate events of reproduction to suitable, narrow windows of time [7,8]
The first important question following the discovery of a lunar rhythm is whether it is controlled by a biological clock and endogenous, or whether it is merely a direct response to external cues in the lunar cycle such as the increased illumination during full moon nights

Summary

Introduction

The intertidal zone of seacoasts, being affected by the superimposed tidal, diurnal and lunar cycles, is temporally the most complex environment on earth. The critical evidence for an endogenous rhythm is that the rhythm must free-run: After being entrained by a specific environmental cue, the so-called zeitgeber, the rhythm must continue under constant conditions, in the absence of that particular cue. This has only been shown for the lunar rhythms of a few species [1,2,3,4,16,17,18,19,20,21]. Such proof is lacking for the coral Acropora millepora and the fish Siganus guttatus, so that their recently-documented transcriptional differences in relation to the lunar cycle [22,23], which represent the only published molecular studies on lunar rhythms to date, cannot necessarily be attributed to a biological clock

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