You look like your mom: parental effects in Atlantic salmon

Van Leeuwen, T.E., McLennan, D., McKelvey, S., Stewart, D.C., Adams, C.E., Metcalfe, N. B. (2016). The association between parental life history and offspring phenotype in Atlantic salmon. J. Exp. Biol. 219: 374-382. doi: 10.1242/jeb.122531

We can all agree that both our personal experiences (nurture) and our genes (nature) have a role in shaping our personality, behaviour, looks, and other traits. The environment you grow up in has a big influence on your talents, interests, and life trajectory. The genes and gene variants you are born with form the basic blueprint of every protein and cell in your body.

But the story is more complicated than nature vs. nurture. The environment the parents experienced during reproduction will also influence the development of their offspring. On a similar note, the environment the parents experienced during their development, and their life history, is also gaining traction as an important predictor of offspring performance and life history pathway.

Parental effects are part of the concept of epigenetics, inheritable traits that are not due to changes in the actual gene or gene variants. Epigenetics are effectively changes in how genes are “read” by cells, and whether they are “on” (active) or “off” (silenced). Such mechanisms are one of the reasons why identical twins, with the same genetic code and raised in the same household, can have very different lifestyles.

Atlantic salmon life history

Atlantic salmon (Salmo salar) spawn in freshwater rivers and streams. Alevin (newly hatched fish with their yolk sac still attached) hide in the gravel for a few weeks, slowly absorbing nutrients from their yolk sac. Once the yolk sac is exhausted, the fish leave the safety of the river bottom and start to feed. They quickly develop into young juveniles called parr, and will grow in their native streams from some time.

Parr typically smolt after 1 to 3 years of growth in their native stream. Smolting is a series of complex physiological and morphological changes that prepare the parr for entering the ocean. As the age of seaward migration is partially determined by growth rate, faster-developing fish spend less time in freshwater. Once at sea, salmon may not return to spawn for years. The amount of time mature salmon spend at sea before returning home to spawn (1 to 6 years) is one source of variation in life history within the population.

Some male fish never smolt and remain stuck in the parr stage. Somehow, these males are able to become sexually mature without migrating seaward. Because of their small size, these “precocious parr” can’t compete directly with the larger, sea-run males during spawning to monopolize mates. Instead, they cruise around the spawning grounds, and participate as sneaker males. Instead of battling for their babes, sneaker males… sneak around spawning pairs and indiscriminately fertilize any eggs they can approach closely. This alternative life history strategy is another source of variation in the population.

Atlantic salmon are excellent models for studying the concept of parental effects in a natural setting because they have multiple potential life histories that not only lead to successful reproduction, but interbreed with each other. Life history routes (e.g. time at sea, sneaker vs. sea-run) in salmon are thought to arise from a mix of genetic and non-genetic factors. Sneaker and sea-run males can develop at the same river site, but go on to lead very different lives.

Life history determination, fish rearing, and metabolism

To investigate how parent life history may influenced offspring traits, Van Leeuwen et al. needed to systematically breed Atlantic salmon with a variety of life history pathways. Mature, sea-run salmon and precocious parr were captured from the River Blackwater, Scotland.

By examining the rings on the scales of their wild-caught breeding fish (a technique called “scalimetry”), the researchers were able to determine the rough age of the each fish, and number of years they had spent in freshwater and saltwater prior to capture. This is because scales grow in a ring-like pattern, producing bands called annuli. Bands are thicker in the summer than in the winter (since they grow faster when food is plentiful), and differ between pre-smolt freshwater and post-smolt seawater salmon.

After capture, the mature females (1 or 2 years at sea) were bred with either sea-run males (1 or 2 years) or sneaker males (0 years at sea). The eggs, separated into family groups, were raised in a hatchery for ~8 months, during which their growth rates and condition were monitored. The following autumn, once the salmon had developed into juveniles (parr), the resting and maximum metabolic rates of the young were tested to get a sense of their overall energy budget and performance. The authors then analyzed the relationships between offspring traits and the life history traits of their parents.

Mother knows best

Mothers that had spent a longer time at sea were larger, and produced larger eggs and larger and stronger offspring at the time of first feeding (even after accounting for the effects of larger egg mass). Marine environments tend to be more productive than freshwater environments, so the larger mothers that spent more time at sea probably have more energy available to invest into their offspring.

Even after accounting for the fact that larger fish tend to hatch out of larger eggs, the relationship between egg mass, maternal life history, and offspring size remained, suggesting difference in other factors, like maternal hormones or individual egg position in the ovary (some eggs are closer to blood vessels and in a better position to received nutrients), may also play a role.

These relationships weren’t as strong once the offspring were no longer dependent on their yolk sacs for nutrients, suggesting maternal investment (and maternal effects) had a major influence on these traits.

While maternal environment leading up to egg production influenced early offspring traits, this study is unable to rule out the influence of genetic effects. Traits that correlated with the father’s life history, such as the greater body condition in sneaker male offspring fry, demonstrate that genetics also has a role in determining offspring traits (since father’s play no role in egg provisioning).

Now when I was your age…

By the time fry had been feeding on their own for some time, the early life history of the mother in freshwater was a better indicator of their developmental trajectory – mothers that left freshwater early produced offspring with higher maximum metabolic rates and aerobic scope, and that grew faster.

The father’s life history also had an effect, though it was less prominent than the role of the mother. Male salmon adopt two major reproductive strategies: the territorial strategy (adopted by sea-run males), where the male defends a single female; and the non-territorial/sneaker strategy, where the male cruises around the spawning ground looking for opportunities to steal fertilizations from larger males.

While both strategies produce viable offspring, no one really knows whether one strategy is more successful than the other in either the quantity or quality of offspring. However, data here suggests that sneaker males produce offspring with relatively high growth rates, in better condition, and maximum metabolic rate (though mother also influenced this). How this shakes down in terms of offspring success and fitness is not known.

Conclusions

The duration of key developmental stages (time in freshwater before seaward migration, length of time at sea before spawning) of the mother, and to a lesser extent the father, are important predictors of offspring metabolic and growth-related traits. It is possible that parents may be adjusting the life history trajectory of their offspring to perform best in the environments that they themselves experienced as juveniles.

Brittney G. Borowiec

Brittney is a PhD candidate at McMaster University in Hamilton, ON, Canada, and joined Oceanbites in September 2015. Her research focuses on the physiological mechanisms and evolution of the respiratory and metabolic responses of Fundulus killifish to intermittent (diurnal) patterns of hypoxia.