Genetic Architecture of Local Adaptation in Lunar and Diurnal Emergence Times of the Marine Midge Clunio marinus (Chironomidae, Diptera)

Abstract

Circadian rhythms pre-adapt the physiology of most organisms to predictable daily changes in the environment. Some marine organisms also show endogenous circalunar rhythms. The genetic basis of the circalunar clock and its interaction with the circadian clock is unknown. Both clocks can be studied in the marine midge Clunio marinus (Chironomidae, Diptera), as different populations have different local adaptations in their lunar and diurnal rhythms of adult emergence, which can be analyzed by crossing experiments. We investigated the genetic basis of population variation in clock properties by constructing the first genetic linkage map for this species, and performing quantitative trait locus (QTL) analysis on variation in both lunar and diurnal timing. The genome has a genetic length of 167–193 centimorgans based on a linkage map using 344 markers, and a physical size of 95–140 megabases estimated by flow cytometry. Mapping the sex determining locus shows that females are the heterogametic sex, unlike most other Chironomidae. We identified two QTL each for lunar emergence time and diurnal emergence time. The distribution of QTL confirms a previously hypothesized genetic basis to a correlation of lunar and diurnal emergence times in natural populations. Mapping of clock genes and light receptors identified ciliary opsin 2 (cOps2) as a candidate to be involved in both lunar and diurnal timing; cryptochrome 1 (cry1) as a candidate gene for lunar timing; and two timeless (tim2, tim3) genes as candidate genes for diurnal timing. This QTL analysis of lunar rhythmicity, the first in any species, provides a unique entree into the molecular analysis of the lunar clock.

Chironomid Midges (Diptera, Chironomidae) Show Extremely Small Genome Sizes

“…1B) can be now considered as having the smallest genome size of any known insect, with a C-value of 0.07 pg DNA, corresponding roughly to 68 Mb. This value is congruent with the genome size of a related species, Clunio marinus, which was estimated once to 95 Mb and more recently to 87.2 Mb (Kaiser and Heckel, 2012;Tobias S. Kaiser, personal communication).…”

“…Thus, small genome sizes should constitute an advantage for chironomid species rapidly developing in temporary environments. Chironomids from the genus Clunio can develop into temporary tide pools and also show synchronized emergence of the adults in relation to the moon cycle and during the short window of the low tide (Kaiser and Heckel, 2012). A high developmental rate should be needed to achieve this.…”

Chronobiology by moonlight

“…Mapping of clock genes and light receptors identified ciliary opsin 2 as a candidate to be involved in both lunar and diurnal timing; cryptochrome 1 (cry1 ¼ 'Insect type' cryptochrome; main photoreceptor of the circadian clock in D. melanogaster) as a candidate gene for lunar timing; and two timeless (tim2, tim3) genes as candidate genes for diurnal timing [93]. tim2 is also called timeout and is involved in chromosome stability and light entrainment of the circadian clock in D. melanogaster [94].…”

“…tim2 is also called timeout and is involved in chromosome stability and light entrainment of the circadian clock in D. melanogaster [94]. The function of tim3 is still unknown, but it has sequence similarities to tim2 and is also present in mosquitoes as Aedes aegypti and Culex quinquefasciatus [93]. The photoreceptor responsible for moonlight detection is most probably located in the larval ocelli [95].…”

Circadian and circatidal clocks control the mechanism of semilunar foraging behaviour

“…In Clunio , experimental studies have identified functional and pigment changes in the larval ocelli 12 together with a photoreceptor pigment (ciliary opsin 2) and a known insect circadian clock gene Cryptochrome1 that are now thought to be associated with the lunar rhythm 13 . Most recently the characterization of the Clunio genome has identified orthologues for the circadian clock genes but these do not yet explain the lunar mechanism 14 .…”