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The early bird gets the worm, part II: How behavioral ecology is connecting the dots between early-life stress and aging

Posted on May 28, 2019 by Kat Munley

This is the second post of a two-part series on a day in the life of a behavioral ecologist, which features the stories and research of members of Dr. Kim Rosvall’s laboratory in the Department of Biology. Click here to read the first post of the series!

In Part I of this series, I discussed how research from the Rosvall lab is shedding light on the biological processes that enable animals to respond to changes in their social environment. Specifically, some members of the Rosvall lab are studying the hormonal mechanisms that females of a local songbird species, called tree swallows (Tachycineta bicolor), use to regulate same-sex aggression across breeding stages and in response to social competition. However, competition is only one of many challenges these animals face during their lives, and some members of the Rosvall lab are studying how temporarily reducing parental care affects offspring development and physiology. This research takes place during the last breeding stage, called the chick provisioning stage (see timeline below), when females are caring for their chicks.

A timeline of different breeding stages is shown in black, which contains tick marks with text that describes each stage. In chronological order (from left to right on the timeline), the stages are territory establishment, mating/egg laying, incubation, and chick provisioning. A blue box with hatch marks is shown over the tick marks for the territory establishment, mating/egg laying, and incubation stages; and a solid red box is shown over the tick marks for the incubation and chick provisioning stages. Black text that reads “Nest Box Manipulations” is located over top of the blue box, between the territory establishment and mating/egg laying breeding stages. Black text that reads “Simulated Territorial Intrusions” is located over top of the blue box, between the mating/egg laying and incubation breeding stages. Blue text that reads “Part I: Seasonal Plasticity in Hormonal Signaling and Territorial Aggression” is located above the black text, and red text that reads “Part II: Effects of Early-Life Stress on Telomere Dynamics” is located over top of the red box.
Timeline of the breeding stages observed in a typical field season in Dr. Kim Rosvall’s laboratory overlaid with descriptions of the topics that will be discussed in this two-part series of posts on a day in the life of a behavioral ecologist. The current post (Part II, in red) discusses the experimental testing that occurs during the late stages of the field season, including the effects of early-life stress on chick development, growth, and physiology. The first post in this series (Part I, in blue) addresses the field manipulations and behavioral assays that are conducted during the early and middle stages of the field season, including nest box manipulations and simulated territorial intrusions.

An adult bird is being held in a person’s hand. The bird’s head is nestled between the person’s index and middle fingers. The bird is holding a small, black insect with wings in its beak. The bird has white feathers on its abdomen and iridescent green and blue feathers on its head and back.
A member of the Rosvall lab holds an adult female tree swallow, who is carrying an insect in her mouth. Adult tree swallows, such as this female, feed their begging chicks a variety of flying insects almost continuously throughout the day for their first few weeks of life. Image credit: Sarah Wolf.

Although female tree swallows are quite aggressive early in the breeding season, they are also faithful mates and caring parents. Once the dust has settled after an initial period of intense competition and females have successfully acquired a territory, they will form a social bond with a single male partner for the entirety of the breeding season. These breeding pairs will build grassy, feather-lined nests in cavities, such as holes in trees and bird boxes, where they will eventually raise their young together as a pair. After a breeding pair mates, the female will lay a single clutch of eggs, which typically consists of 4-7 chicks that will all hatch within a day of one another. For several days after the chicks first hatch, the female will also spend a lot of time warming her chicks, since at this point, the chicks are unable to thermoregulate, or warm themselves. In addition, both parents will feed their begging chicks a variety of flying insects, like flies and mosquitos, almost continuously throughout the day for their first few weeks of life. During this concentrated growth period, chicks grow in size by 20-fold, approaching their adult mass around 12 days old. Then, about a week later, the chicks will fledge the nest, and they will soon forage on their own for the first time.

A group of five small chicks is sitting in a nest lined with white and gray bird feathers, which is lying in a wooden nest box. The chicks are exhibiting begging behavior and have their mouths open and pointed towards the sky. The chicks are mostly gray in color, except for the inside of their mouths, which are yellow, and their undersides, which have some spots of light pink skin showing under their feathers.
A brood of tree swallow chicks begs for food from their parents. This begging behavior is commonly observed in growing chicks, and their parents will feed them insects almost continuously throughout the day during the chick provisioning stage. Unfortunately, aspects of parental care, such as feeding, are typically compromised in adult tree swallows that experience environmental or social stressors. Image credit: Dr. Kim Rosvall.

The chick provisioning stage of the breeding season seems simple enough: adult tree swallows care for their young for a few short weeks, and their chicks eventually fledge the nest. However, there are a suite of stressors that could interfere with this seemingly straightforward process. For example, adult tree swallows face both environmental challenges, such as fluctuations in temperature, and social pressures from other tree swallows, such as competition. Oftentimes, adults will adapt to these environmental and social pressures by reducing parental care, since during stressful situations, parents may divert their energy inwards to ensure their own survival. Unfortunately, this reduction in parental care could have serious consequences on their offspring, since chicks are entirely dependent on their parents for nourishment and nurturing during this critical period of development.

A young, smiling adult woman is handling an adult bird in her right hand. She is holding the bird’s head between her index and middle finger. The bird has white feathers on its abdomen and iridescent green and blue feathers on its head and back.
Rosvall lab graduate student Sarah Wolf holds an adult tree swallow at one of her field sites. Sarah’s research focuses on how telomere dynamics and behavioral plasticity are linked, specifically in response to social and environmental stressors. Image credit: Sarah Wolf.

So, what physiological changes might occur in offspring that experience short-term reductions in parental care, such as those induced by stress? Graduate student Sarah Wolf is particularly interested in how temporary reductions in maternal care can affect offspring stress reactivity and cellular aging. Sarah addresses these questions by measuring the offspring’s telomeres, regions of repetitive DNA sequences located at the end of chromosomes, or molecules that carry an organism’s genetic material. Telomeres can be thought of as the plastic ends of shoelaces; they not only protect our chromosomes, or “shoelaces,” from deteriorating, but they also prevent chromosomes from unraveling and fusing together. Although telomere length naturally tends to shorten with age, studies have shown that stress accelerates this process. In other words, stress elevates telomere shortening by damaging both the telomeres themselves and the chromosomes they are protecting. Thus, for tree swallows and other wild animals, telomeres could be the key to predicting offspring survival and how good of a parent these individuals will be during adulthood.

A young bird is perched on top of a person’s fingers. The bird has white feathers on its abdomen and gray feathers on its back.
A 12 day old tree swallow chick perches on top of a Rosvall Lab member’s fingers. This individual is growing in size and developing gray feathers in preparation for fledging the nest. Later on, this tree swallow will molt to acquire vibrant, blue-green iridescent feathers that are characteristic of these colorful songbirds. Image credit: Sarah Wolf.

To test the effects of early-life stress on telomere dynamics and to assess whether telomere length can predict how well individual offspring cope with a stressor, Sarah treated tree swallow mothers with lipopolysaccharide (LPS), a mild immunological stressor that produces characteristic symptoms of sickness without physically making the animals ill. In turn, these females reduced how much they provisioned their offspring for just one day, similar to how they would respond to a natural short-term illness. Then, Sarah and other members of the Rosvall lab sampled and monitored the chicks throughout development to see how a temporary reduction in maternal care affects growth rate, stress tolerance, and telomere dynamics throughout the chick provisioning period. While Sarah’s research is ongoing, her results thus far suggest that early-life stress does influence offspring stress reactivity and telomere dynamics, but it does not affect physical traits. Surprisingly, chicks cared for by a LPS-treated mother were more likely to elongate their telomeres in response to treatment relative to control chicks. Interestingly, Sarah also found sex differences in these measures, where male chicks were more likely to exhibit telomere shortening and were less likely to survive to fledging and return to their breeding grounds the following season compared to female chicks. In other words, while both male and female LPS chicks elongated their telomeres in response to reduced maternal care, this change was less pronounced in male LPS chicks than in female LPS chicks.

Together, Sarah’s findings show that a tiny, short-term stressor, in the form of a few hours of lower feeding rates, can profoundly impact chick physiology and survival, especially in males. If chicks show such prominent physiological changes after only a few hours of stress, one can only imagine how long-term environmental stressors, such as a week-long rainstorm or a cold snap, could affect these chicks’ survival and ability to cope with stress. While these possibilities are daunting, there is still hope: Sarah’s data also suggest that chicks may be capable of enacting protective mechanisms that can buffer them from these acute stressors. However, it is still unknown whether these adaptations are strong enough for chicks to survive until the next breeding season, a question that Sarah will explore further in her own research.

Acknowledgments: I would like to thank Dr. Kim Rosvall and Sarah Wolf for sharing their passion for research with me and for their thoughtful comments on this post.

Edited by Riddhi Sood and Katherine VanDenburgh

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Filed under: Cutting-Edge Science at IU, Spotlight on PeopleTagged aging, animal behavior, Biology, development, Ecology, endocrinology, field research, stress

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