Genetic correlation between the pre-adult developmental period and locomotor activity rhythm in Drosophila melanogaster

Abstract

Biological clocks regulate various behavioural and physiological traits; slower circadian clocks are expected to slow down the development, suggesting a potential genetic correlation between the developmental period and circadian rhythm. However, a correlation between natural genetic variations in the developmental period and circadian rhythm has only been found in Bactrocera cucurbitae. The number of genetic factors that contribute to this genetic correlation is largely unclear. In this study, to examine whether natural genetic variations in the developmental period and circadian rhythm are correlated in Drosophila melanogaster, we performed an artificial disruptive selection on the developmental periods using wild-type strains and evaluated the circadian rhythms of the selected lines. To investigate whether multiple genetic factors mediate the genetic correlation, we reanalyzed previously published genome-wide deficiency screening data based on DrosDel isogenic deficiency strains and evaluated the effect of 438 genomic deficiencies on the developmental periods. We then randomly selected 32 genomic deficiencies with significant effects on the developmental periods and tested their effects on circadian rhythms. As a result, we found a significant response to selection for longer developmental periods and their correlated effects on circadian rhythms of the selected lines. We also found that 18 genomic regions had significant effects on the developmental periods and circadian rhythms, indicating their potential for mediating the genetic correlation between the developmental period and circadian rhythm. The novel findings of our study might lead to a better understanding of how this correlation is regulated genetically in broader taxonomic groups.

Correlated changes in life history traits in response to selection for faster pre-adult development in the fruit fly Drosophila melanogaster

“…Correlation between development time and circadian clocks was also reported in laboratory selection studies on melon flies (Miyatake, 1997b;Shimizu et al, 1997) and fruit flies (Kumar et al, 2006;Takahashi et al, 2013;Yadav and Sharma, 2013a). Disruption of circadian timing systems results in reduced reproductive output in the gypsy moth, Lymantria dispar (Giebultowicz et al, 1990), and D. melanogaster (Beaver et al, 2002;Beaver et al, 2003), shortening of adult lifespan in D. melanogaster (Hendricks et al, 2003;Kumar et al, 2005), reduction in vegetative growth and survivorship in Arabidopsis thaliana (Dodd et al, 2005), and increased predation in free-living ground squirrels Spermophilus lateralis (DeCoursey et al, 1997) and chipmunks Tamias striatus (DeCoursey et al, 2000).…”

Pace‐of‐life: Relationships among locomotor activity, life history, and circadian rhythm in the assassin bug,Amphibolus venator

“…For example, strains of the melon fly Bactrocera cucurbitae artificially selected for a shorter developmental period had shorter free-running periods of circadian rhythm than did strains selected for a longer developmental period (Shimizu, Miyatake, Watari, & Arai, 1997). The same phenomenon was also seen in Drosophila melanogaster (Kumar, Kumar, Paranjpe, Akarsh, & Sharma, 2007;Takahashi, Teramura, Muraoka, Okada, & Miyatake, 2013). These studies suggest correlations between life history traits and the free-running period of circadian rhythm.…”

Extent of mismatch between the period of circadian clocks and light/dark cycles determines time‐to‐emergence in fruit flies

“…Circadian ( circa = about ; dies = a day ) clocks with near 24‐h periodicities regulate behavioral and metabolic processes in a wide variety of organisms (Saunders, ; Dunlap et al ., ). In insects including fruit flies Drosophila melanogaster , these clocks have also been implicated in the regulation of life‐history traits such as preadult development time and adult lifespan (Kyriacou et al ., ; Miyatake, , ; Shimizu et al ., ; Klarsfeld & Rouyer, ; Sheeba et al ., ; Paranjpe et al ., ; Takahashi et al ., ; Yadav & Sharma, 2013, 2014). It is believed that preadult development time of flies with faster circadian clocks is shorter than those with slower clocks.…”

“…It is believed that preadult development time of flies with faster circadian clocks is shorter than those with slower clocks. While this proposal still awaits rigorous and unequivocal empirical support, previous studies in fruit flies D. melanogaster (Kyriacou et al ., ; Paranjpe et al ., ; Kumar et al ., ; Takahashi et al ., ; Yadav & Sharma, 2013), and in melon flies Bactrocera cucurbitae (Miyatake, , ; Shimizu et al ., ) have shown that the period of circadian activity/rest rhythm is correlated with the egg‐to‐adult duration.…”

“…Correlation between τ and preadult development time has also been reported in studies on wild‐type fly populations selected for differences in their preadult developmental duration (Miyatake, , ; Shimizu et al ., ; Takahashi et al ., ; Yadav & Sharma, 2013), or for morning and evening adult emergence (Kumar et al ., ). For example, in a study on melon flies B. cucurbitae , populations selected for shorter preadult development time were found to have faster running clocks ( τ ∼ 22.6 h) and advanced time of mating, while those selected for longer development time have slower running clocks ( τ ∼ 30.9 h) and delayed time of mating (Miyatake, , ; Shimizu et al ., ).…”