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

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 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.

Polygenic adaptation from standing genetic variation allows rapid ecotype formation

“…This leads to an inevitable phenotyping error for a fraction of individuals. However, in another study, we could show that this phenotyping error does not impede the detection of an oligogenic genetic architecture in QTL mapping for a comparable arrhythmic phenotype ( Briševac et al, 2022 ). As a control that in principle we had sufficient power for QTL mapping in this crossing family, we also mapped the sex determining locus, which was clearly detectable ( Figure 4 ).…”

“…Lunar emergence times were recorded by counting the number of emerged midges in the laboratory cultures every day over several months and summing them up over several tidal turbulence cycles. Emergence data for He-1SL was taken from Neumann, 1983 , emergence data for Por-1SL was taken from Briševac et al, 2022 .…”