Eggs With Attitude: The Behavior of Bluebirds
Mother bluebirds influence their male chicks while they are still in the egg, thus shaping the ecological communities in which they will live, a UA-led research team reports in a paper published in the journal Science.
Depending on the level of competition they experience during nesting season, female bluebirds allocate different amounts of hormones into their eggs, producing sons that are more or less competitive, which in turn influences the dispersal behavior of subsequent generations, a team led by University of Arizona biologists has discovered.
"Mothers are uniquely positioned to be a bridge between current environmental conditions and the traits of their offspring," said Renée Duckworth, an assistant professor in the Department of Ecology and Evolutionary Biology in the UA College of Science. "This is one of those rare cases where we can see how these local behavioral interactions, which can be exceptionally variable, can lead to highly predictable ecological patterns on a large scale."
While scientists have long known that females of many animal species provide their offspring with much more than their genes — nutrients, hormones and other valuable ingredients for life — few examples have been documented in which the maternal contribution to offspring generation directly shapes their environment and interactions with other species on a large, landscape-wide level.
The study, published in the journal Science, provides the first detailed understanding of how environmental conditions can directly influence behavioral patterns across generations, behaviors that in turn lead to one species replacing another in ecological communities.
Duckworth leads a research group that addresses how interactions among individuals scale up to affect broader ecological processes such as changes in species assemblages.
"We want to know how understanding the lower-level mechanisms help you make sense of higher-level patterns as you go from the small scale of individuals interacting to the large scale of entire populations and landscapes," she said.
To find answers, the team studied populations of western bluebirds and mountain bluebirds, two closely related species that compete for nesting cavities in patches of forest recently ravaged by wildfires. Because bluebirds depend on those habitats as their prime nesting grounds, members of both species are in intense competition with each other and also with birds of other species looking to colonize the same spaces.
Mountain and western bluebirds compete for nest cavities in post-fire forests — a successional habitat that lasts for roughly 20 bluebird generations. Bluebirds must be able to continually recolonize newly available post-fire habitat to survive. This leads to cycles of species replacement: Mountain bluebirds are more dispersive and find new habitat first, whereas western bluebirds are more aggressive and can displace other species once they show up. Once western bluebirds displace mountain bluebirds, they go through a rapid decline in aggressive behavior until the cycle is reset by fire.
"We had some evidence there was a maternal effect that influenced variation in aggression of offspring that we observed," Duckworth said. "We knew that if a son develops in eggs laid earlier, he is more aggressive compared to sons hatching from later eggs. But we didn't know why birth order influences aggression, and why mothers produce sons early or late."
Duckworth and her colleagues suspected that the mothers' response to different resource environments was driving these cycles in the post-fire habitats, but they needed to collect data from the individual all the way up to the population level at multiple populations across different stages of species replacement.
To determine how nest cavity resources influenced the maternal effects, the researchers separated the territories into two groups: one that had only a single nest cavity up for grabs, and randomly selected other territories, which they provided with additional nest boxes. They then recorded how the females behaved, as they were beleaguered by other bluebirds, wrens or tree-swallows, the most dominant competitor. During such competitive interactions, the researchers also measured hormonal allocation of these females into their developing eggs and the effects such allocation had on behavior of resulting offspring.
"If the bluebird females had only one cavity, they had to continuously fend off the other competitive species," Duckworth said. "But if they have a lot of nest cavities on their territory, they don’t fight as often because other species don't try to steal their primary nest cavity as much."
Establishing these behavioral differences was key to understanding how information about changes in resource availability could be transmitted to offspring.
Duckworth and her team studied hundreds of nests across populations that were at different stages during the population cycle and studied what maternal effects were at work at each stage. The scientists then combined that data with a long-term study done over 11 years and measured hormone allocation in the naturally varying bluebird populations.
They discovered that when western bluebirds experienced a lot of competition, they allocated more androgens to their clutches. As a result, sons hatching from these eggs were more aggressive and more likely to disperse farther and colonize new areas. Once there, they establish large territories and drive out resident populations of mountain bluebirds.
On the other hand, if the females experienced very little competition, they allocated low levels of androgens to eggs, producing "stay-at-home" sons that were less aggressive and more likely to obtain a territory near their parents' nest.
"The older a population, the more crowded it gets," Duckworth said. "This translates to smaller territory size, and that's OK if you have your relatives next to you, but not if you're facing fierce competition from strangers."
In the greater scheme of things, Duckworth's research has implications that go far beyond the world of ecological interactions.
"There is mounting evidence from medical research that the environment to which a pregnant mother is exposed can determine the stress response of the offspring for rest of its life," said Duckworth, who recently received a $750,000 CAREER grant, the National Science Foundation's most prestigious award in support of faculty who exemplify the role of teacher-scholars through outstanding research, excellent education, and the integration of education and research within the context of the mission of their organizations.
"We will use this support to follow up on results we obtained in this and in other studies," Duckworth said. "We are excited to start looking at eco-evolutionary dynamics in this system, which is how changes in behavior are driven by rapid evolutionary changes or demographic effects.
"There is a heritable variation in and natural selection on aggression in this system, and our goal is to see how maternal effects play into the mix and to tease apart the relative importance of all of these in long-term evolution."
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