UC Davis researchers led by molecular geneticist and physiologist Joanna Chiu, vice chair of the Department of Entomology and Nematology, have identified a key driver in how animals “sense” seasonal changes.   

The paper, appearing online on the website of the Proceedings of the National Academy of Sciences (PNAS), solves a puzzle that scientists have tried to piece together for a long time.   

The Chiu lab did it with the widely used model organism, Drosophila melanogaster, also known as the vinegar fly. 

“This paper advances our understanding of how animals ‘sense' seasonal changes in day length and temperature to modulate their physiology and behavior in order to survive through seasonal variations in their environment,” Chiu said. “Specifically, we identified the protein EYA to be a key driver of seasonal changes in biology. By manipulating the level of EYA protein using transgenic technologies in specific neurons of the vinegar fly Drosophila melanogaster, we were able to disrupt the fly's ability to sense seasonal changes.” 

“We were able to trick them into thinking that it is winter when it is actually summer time and vice versa,” Chiu said. “Interestingly, this protein is very conserved in other animals, including in birds and mammals, suggesting that the mechanism we are studying could be widely used in the animal kingdom.” 

The paper, “EYES ABSENT and TIMELESS Integrate Photoperiodic and Temperature Cues to Regulate Seasonal Physiology in Drosophila,” is the work of the first author and postdoctoral fellow Antoine Abrieux, graduate students Yao Cao and Kyle Lewald, undergraduate researcher Hoang Nhu Nguyen, in collaboration with members of Dr. Yong Zhang's lab at the University of Nevada Reno. Associate Professor Joanna Chiu is the corresponding and senior author. 

“There is still a lot of work to be done in order to understand how the EYA protein regulates seasonal physiology and behavior,” said Chiu, who was named one of 10 UC Davis Chancellor's Fellows in January 2019, “but we are excited that our work opened up a lot of new interesting questions.” 

In their abstract, the seven-member team wrote: “Organisms possess photoperiodic timing mechanisms to detect variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that, in Drosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation of eya expression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically, we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in female D. melanogaster.”

“Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations that tim null mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressing tim show an increased incidence of reproductive dormancy even in long photoperiod.” 

Research in the Chiu lab focuses on the regulation of biological rhythms and their control over organismal physiology. Her expertise involves molecular genetics of animal behavior, circadian and seasonal biology, and posttranslational regulation of proteins. 

By using Drosophila melanogaster as a model to study the mechanisms that regulate circadian clocks, Chiu has discovered new insights into the function of key proteins that control animal circadian clocks. She earlier identified new mechanisms that slow down or speed up the internal clock of vinegar flies and mechanisms that allow the internal clock to interpret food as timing cues--research that could help lead the way to alleviate human circadian and metabolic disorders. 

“Besides being indispensable for the control of daily activities in animals, such as the sleep-wake cycle, locomotor activity, hormone circulation and food intake, defects in circadian rhythms and clock genes have also been implicated in a wide range of human disorders, including chronic sleep orders, various forms of depression, metabolic syndromes, as well as susceptibility to cancer and drug and alcohol addiction,” Chiu says. 

D. melanogaster is widely used for biological research due to its rapid life cycle, simple genetics (only four pairs of chromosomes), and its large number of offspring per generation, according to Wikipedia. As of 2017, six Nobel prizes had been awarded for research using Drosophila. 

The fly, a member of the family Drosophilidae, is a nuisance pest found worldwide in restaurants and other places where food is served.

First author and postdoctoral fellow Antoine Abrieux, an international scholar from France, holds a doctorate from Angers University,  France. He joined the Chiu lab in spring 2016 to explore interactions between the clock and endocrine system underlying seasonal adaptation in Drosophila suzukii. He discussed his work at a UC Davis Department of Entomology and Nematology seminar in February 2019 about the molecular mechanisms involved in seasonal adaptation in insects.

DAVIS--Monarch genetics expert Christine Merlin, assistant professor in the Department of Biology, Texas A&M University, will speak on "The Monarch Butterfly Circadian Clock: from Clockwork Mechanisms to Control of Seasonal Migration" from 12:10 to 1 p.m., Wednesday, June 1 in Room 230 of Wellman Hall.

The seminar, sponsored by the UC Davis Department of Entomology and Nematology, will be hosted by assistant professor Joanna Chiu.

Merlin joined Texas A&M's Department of Biology in the fall of 2013 and is a member of the Center for Biological Clocks Research. 

The eastern North American monarch butterfly (Danaus plexippus) has emerged as a powerful model system to study animal circadian clocks and their role in an unconventional output, the photoperiod-induced long-distance migration," Merlin says in her abstract.

"Circadian clocks are endogenous 24-hour timekeepers that coordinate nearly all of the animal physiology and behavior to its environment to tune specific activities at the most advantageous time of the day. Monarchs use a circadian clock to navigate to their overwintering sites during their seasonal long-distance migration. The clock time-compensates for the movement of the sun across the sky over the course of the day and regulates the sun compass output in the brain. Circadian clocks could also be used to time the monarch seasonal departure from their breeding grounds, and consequently regulate the genetic/epigenetic program controlling migratory physiology and behavior."

"I will discuss progress that our lab has made in developing reverse-genetics in the monarch butterfly to unlock its potential as a genetic model system to study animal clockwork mechanisms and the involvement of the circadian clock in insect photoperiodic responses," she says. "And if we can show this is the case and that the circadian clock is involved, we can now start to understand the genetic program that is allowing the migratory behavior."

In a news story written by Vimal Patel of the Texas A&M communications office, Merlin is described as zeroing in on "unraveling the mysteries of the migration and the role of internal clocks in the process."

Merlin was quoted as saying: "It's incredible how such a fragile insect can complete a long-range migration so demanding. Every piece of it fascinates me, from how it occurs to why they go precisely where they go."

An excerpt from Patel's piece:
"While she was a postdoctoral researcher at the University of Massachusetts Medical School in the laboratory of Prof. Steven Reppert, Merlin and colleagues showed that the clocks necessary for flight orientation lie in the creatures' antennae -- a departure from the previous conventional wisdom that the brain controlled the mechanism, given that it controls behavioral rhythmicity in virtually every other animal, including humans.

"The conclusion stemmed from Merlin's and her co-workers' collective curiosity concerning a decades-old anecdote. Around 50 years ago, entomologist Fred Urquhart found that Monarchs became disoriented after he clipped off their antennae. Since then, it had remained just a suspicion until the Massachusetts team confirmed it with more rigorous research."

"The team's experiment exploited technology in a way Urquhart, who merely observed the Monarchs in flight, could not at the time. They used a plastic barrel-like device called a Mouritsen-Frost flight simulator in which a butterfly is connected by tungsten wire to an output system that indicates which direction it is flying. The results were clear: The antennae-less Monarchs flew in every which direction, while those with intact antennae flew southwesterly, the migratory direction."

Merlin says she's interested in the role of the circadian clock in the induction of the migration. "Migration begins every year in the fall, when the day lengths change," she says. "The shortened day lengths might be a cue for the monarchs to start their migration. And if we can show this is the case and that the circadian clock is involved, we can now start to understand the genetic program that is allowing the migratory behavior."

A native of France, Merlin received her bachelor's, master's and doctoral degrees majoring in animal biology, invertebrate physiology and insect physiology, respectively, at the University Paris 6 Pierre and Marie Curie in France. She accepted a postdoctoral fellowship at the University of Massachusetts in 2007.

Related Links:

• Christine Merlin Lab
• A recent story involved Merlin's partnership with the Texas A&M Center for Mathematics and Science Education's Craig Wilson, along with local mayors and resident monarch enthusiasts within the Bryan-College Station community.