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Genetic analysis of a phenotypic loss in the mechanosensory entrainment of a circalunar clock.

Authors :
Briševac, Dušica
Prakash, Celine
Kaiser, Tobias S.
Source :
PLoS Genetics; 6/22/2023, Vol. 19 Issue 6, p1-31, 31p
Publication Year :
2023

Abstract

Genetic variants underlying traits that become either non-adaptive or selectively neutral are expected to have altered evolutionary trajectories. Uncovering genetic signatures associated with phenotypic loss presents the opportunity to discover the molecular basis for the phenotype in populations where it persists. Here we study circalunar clocks in populations of the marine midge Clunio marinus. The circalunar clock synchronizes development to the lunar phase, and it is set by moonlight and tidal cycles of mechanical agitation. Two out of ten studied populations have lost their sensitivity to mechanical agitation while preserving sensitivity to moonlight. Intriguingly, the F1 offspring of the two insensitive populations regained the sensitivity to mechanical entrainment, implying a genetically independent loss of the phenotype. By combining quantitative trait locus mapping and genome-wide screens, we explored the genetics of this phenotypic loss. QTL analysis suggested an oligogenic origin with one prevalent additive locus in one of the strains. In addition, it confirmed a distinct genetic architecture in the two insensitive populations. Genomic screens further uncovered several candidate genes underlying QTL regions. The strongest signal under the most prominent QTL contains a duplicated STAT1 gene, which has a well-established role in development, and CG022363, an ortholog of the Drosophila melanogaster CG32100 gene, which plays a role in gravitaxis. Our results support the notion that adaptive phenotypes have a complex genetic basis with mutations occurring at several loci. By dissecting the most prevalent signals, we started to reveal the molecular machinery responsible for the entrainment of the circalunar clock. Author summary: Biological clocks allow organisms to synchronize their physiology and behaviour with their environment. A key part of this mechanism are reliable environmental cues that play a role in setting the clock. Here we study the circalunar clock of Clunio marinus, a marine insect that inhabits the intertidal zone. The circalunar clock is set by moonlight as well as mechanical agitation caused by the tides. Interestingly, in two out of ten studied Clunio populations, mechanical agitation was not sufficient to set the circalunar clock. We found that this loss of sensitivity has a genetic basis. Furthermore, we use the insensitive populations as natural mutants. Finding the mutations that lead to the loss of sensitivity allows us to uncover the molecular mechanisms underlying the setting of the yet unexplored molecular clockwork. Additionally, by uncovering the genetic basis for the loss of sensitivity in two independent populations, we get insights into the processes underlying the evolutionary adaptation of biological clocks. [ABSTRACT FROM AUTHOR]

Details

Language :
English
ISSN :
15537390
Volume :
19
Issue :
6
Database :
Complementary Index
Journal :
PLoS Genetics
Publication Type :
Academic Journal
Accession number :
164461209
Full Text :
https://doi.org/10.1371/journal.pgen.1010763