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The loss of circalunar rhythms in arctic and tide-free habitats: genomic investigations into lunar-arrhythmic populations of Clunio marinus


Fuhrmann,  Nico
IMPRS for Evolutionary Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;
Max Planck Research Group Biological Clocks, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Fuhrmann, N. (2022). The loss of circalunar rhythms in arctic and tide-free habitats: genomic investigations into lunar-arrhythmic populations of Clunio marinus. PhD Thesis, Christian-Albrechts-Universität, Kiel.

Cite as: https://hdl.handle.net/21.11116/0000-000A-0252-7
Biological rhythms are adaptations to periodically changing environmental conditions.
The non-biting midge Clunio marinus (Diptera: Chironomidae) is known for the link
between its reproduction and the tidal regime. The short-lived adults emerge when most
of the intertidal habitat is exposed. The spring low tides occur at location specific times
on days around the full moon and new moon. C. marinus populations at the European
Atlantic coast are locally adapted to the day time and lunar phase of the spring low tides.
This timing is achieved through the combination of an circadian and circalunar rhythm.
While the circadian rhythm is controlled by a transcriptional-translational feedback loop,
the molecular workings of the circalunar rhythm are not understood yet.

As tides are almost neglectable in the Baltic Sea, the local Clunio populations have
adapted to lay the egg clutches in the open sea instead of an exposed intertidal substrate.
This simultaneously removed the selective pressure to time the reproduction to the lunar
phase and allowed for lunar-arrhythmic emergence throughout the entire mating season.
In arctic habitats of the Atlantic coast tides are still present. During the mating season
the sun illuminates the habitat around the clock, preventing the perception of moon light.
C. marinus changed from circadian-circalunar-controlled emergence to circatidal rhythms
in polar day conditions. The adults emerge every day at every low tide throughout the
mating season. In my thesis, I investigated these cases of lunar-arrhythmicity in Northern
European Clunio populations. By exploring the genetic features linked to the evolution
of the here described ecotypes of C. marinus, we step further towards understanding the
enigmatic circalunar rhythms. My investigations resulted in one published article, one
published preprint and an additional chapter.

The first article had two aims: First, I investigated the ability of short mitochondrial
fragments to recover the whole mitochondrial biogeography of geographically distinct pop-
ulations. DNA barcodes are short, conserved genomic fragments and commonly used to
reconstruct the biogeography of species. With my Clunio populations as example I wanted
to point out what issues can arise from blindly using those highly conserved DNA frag-
ments. The second aim was to get the basic mitochondrial biogeography of all distinct
population as a foundation to the investigations into the evolution of lunar-arrhythmic
ecotypes. My second chapter is separated into two parts. At first I take a look at the evolution
of lunar-arrhythmicity in the studied populations. Population structure and admixture
analyses in addition to the mitochondrial biogeography were combined to identify the his-
torical scenario which lead to the evolution of lunar-arrhythmic populations. Secondly, I
used direct genomic comparisons to find differentiated regions and adaptive loci between
rhythmic populations from the Atlantic coast and the arrhythmic populations from the
Baltic Sea specifically. Established laboratory cultures of two sympatric populations were
crossed for further insight into the nature of the maintenance of both populations under
gene flow. In my article I identify genetic variants differentiated between lunar-rhythmic
and lunar-arrhythmic populations. Genetic clusters affected by those genetic variants com-
prise genes for the control of circadian rhythms, neuronal development, mating behavior,
responses to hypoxia and sodium ion transport.

In my third chapter I performed a crossing experiment to identify putative genotypes
linked to lunar-rhythmic phenotypes. By crossing two sympatric populations with differ-
ing ecotypes, I was able to raise an F2 generation with a mix of rhythmic and arrhythmic
phenotypes. With the use of PCR-primers designed specifically for differentiated regions
between the grandparent genomes I obtained genotypes for six distinct loci per chro-
mosome of 237 individuals. The QTL analysis revealed multiple significant loci on all
chromosomes with nine investigated phenotypes linked to lunar-rhythmicity.

My thesis takes a large step towards the understanding of the circalunar rhythms
in C. marinus by comparing rhythmic to naturally occurring arrhythmic populations. I
generated a comprehensive genomic resource for geographically and ecologically distant
populations of the same species. Genomic screens for ecotype-adaptive loci identified a
putative involvement of circadian clock genes in circalunar rhythms of C. marinus. A
crossing experiment between rhythmic and arrhythmic ecotypes of the sympatric Bergen
populations hinted towards the involvement of multiple loci across the genome in lunar-
rhythmicity. The addition of further genetic markers could identify a link of the circadian
clock to circalunar rhythms as well as unravel the maintenance of sympatric ecotypes.