Fish dads offer new insight into behavioral effects of receiving paternal care

UNIVERSITY PARK, Pa. — The plot of "Finding Nemo," a film that features an overprotective single father fish taking on dangers at sea to care for his son, may be more reflective of actual fish dad behavior than was previously known. A new study led by a scientist at Penn State found that baby freshwater fish, when raised by dutiful fathers, fare far better than their non-dad-raised peers in life-or-death situations.

After conducting a novel study that included both behavioral observations and brain genomics analyses, the researchers concluded that early paternal care was associated with later behavioral differences and changes in brain gene regulation. The researchers recently reported their findings in Philosophical Transactions B of the Royal Society.

When the team led by Jason Keagy, associate research professor of wildlife behavioral ecology in Penn State’s College of Agricultural Sciences, was looking for insight into whether the care a baby receives from its father early in life changes how it behaves later in life, they chose an unusual species to study: threespine stickleback fish. The small fish — adults typically are less than 3 inches long — are native to most waters in northern latitudes, and they have one important quality.

Only stickleback fathers provide care to their offspring. Stickleback mothers do not provide any post-laying parental care; instead, they lay their eggs in the male's nest and immediately leave the territory.

The researchers found that the fish that had received paternal care tended to behave in ways they interpreted as having greater boldness and sociability. And the team reported that paternal care affected brain gene expression.

“Having their father around during the first 10 days appeared to influence how the fish behaved later in life,” said Keagy, the study’s first author.

By far, most of the research on parental-care effects that has been done with model organisms has been conducted with mice and rats — which are very maternally driven, Keagy noted. Behavioral scientists don’t understand the effects of fathers as well as those of mothers, he explained, so they turned to sticklebacks.

When it comes to parenting, fish brains share surprisingly similar deep hormonal and genetic building blocks with human brains, despite lacking the same complex outer cortical structure, Keagy pointed out.

“Sticklebacks are one of the rare species in which fathers exclusively take care of the babies, so it’s a good system to study to try to understand what aspects are changed when a different parent is in charge,” he said. “Eventually, we can leverage that knowledge to better understand parental care in general, and ultimately, it may give us insight into the many human problems that come about because of deficient parental care. And conversely, it may help us appreciate the aftereffects of really good parental care.”

In the study, the researchers used a “half-sib design,” meaning they had offspring that shared the same father but had different mothers. This helped them separate effects caused by the father’s care from effects caused by genetics. The team divided the baby sticklebacks into two early-life conditions: a paternal-care group in which babies were raised by their fathers for the first 10 days — the normal period of paternal care for sticklebacks; and an orphaned/hand-reared group, in which the babies were removed from their fathers and raised by researchers for those 10 days.

After that, all of the fish were raised in the same environment. Sometimes referred to as a common garden, that environmental condition allowed the researchers to reasonably determine later behavioral differences were related to those first 10 days of paternal care.

As the fish grew, the team tested them in three situations. First, in an “open-field test,” the fish were placed in a relatively unfamiliar, open environment and exposed to a simulated predator attack. Their reaction told the researchers about their boldness or fearfulness.

“A fish that is willing to explore or remain active despite danger may be considered more bold,” Keagy said.

Next was a social behavior test. The team monitored how the young fish interacted socially with one another, again with a simulated predator attack. This yielded information about sociability and responses to danger in a social context, Keagy explained.

Third, the researchers administered a light–dark test, in which fish were exposed to areas with different lighting.

“This scenario is commonly used to study anxiety-like or exploratory behavior,” Keagy said. “Animals often have different preferences for dark versus brightly lit areas.”

In each of the three experiments, the researchers found that the fish that had received paternal care seemed bolder, more sociable under stress and more adventurous.

Finally, the team looked at the fishes’ brains, focusing on two things. They evaluated gene expression — which genes were being used or were “switched on” — and chromatin accessibility, a molecular measurement that gave the researchers clues about which parts of the genome are available for regulation and potentially gene activation.

The researchers found large effects of paternal care treatment on brain gene expression in offspring. Nearly 10% of individual genes and nearly 15% of gene expression modules — groups of genes with similar expression patterns that work together in biological processes — were differentially expressed long after differences in paternal care were experienced. Taking into account other environmental factors, the only experience that differed consistently between half-sibs from different care treatments was whether they experienced paternal care for 10 days.

“So, it is likely that the time when stickleback offspring are receiving paternal care is also an important developmental period when they are especially sensitive to certain stimuli,” Keagy said. “These results suggest that paternal care is associated with differences in brain gene regulation that affect brain development and function, which result in differences in adult behavior.”

Alison Bell, interim associate dean for research, Department of Evolution, Ecology and Behavior, School of Integrative Biology, University of Illinois at Urbana-Champaign, contributed to the research.

This work was supported by the National Institutes' of Health's National Institute of General Medical Sciences under grant number R01GM082937 and by the U.S. Department of Agriculture’s National Institute of Food and Agriculture under project PEN04768 and accession number 1026660. This content is solely the responsibility of the authors and does not necessarily represent the views of the funders.