Parallel Evolution of Avoidance Behaviors Exhibited by Freshwater and Marine Sticklebacks

By: Moussa Abboud, Victoria Pinaretta, Jack Ryan, and Cameron Sarkisian (Stonehill College, BIO323: Evolution, Spring 2023)

Just as natural selection acts on land, the creatures of the sea experience the same selective pressures! As a mode of evolution, natural selection works by weeding out those who are not as fit as others, while promoting those who are most successful at survival and reproduction. If the history of evolution has taught us anything, it is that one important way to make sure your genes get passed on through your offspring is to become the best at adapting to your environment! A great example of such a concept is visualized in nine-spined sticklebacks (Pungitius pungitius), where the predatory avoidance behaviors of freshwater and marine populations provide insight into the differences in how they evolved this behavior from a common ancestor. Here, we summarize an article about these sticklebacks that was published recently in Evolution by researchers from the University of Helsinki.

A short podcast summarizing the article

The goal of this study was to determine if genetically linked behaviors could evolve through natural selection (differences in survival and reproduction due to differences in appearance phenotype) and, if so, whether those behavioral traits are well-suited to apply to local adaptation in general. The behaviors of interest studied in the article were antipredator behaviors exhibited by marine and freshwater sticklebacks, which would thereby dictate the level of phenotypic plasticity between these two different stickleback populations. Phenotypic plasticity is the ability of a single genotype (genetic composition) to produce multiple different phenotypes (observable characteristics of an individual) when exposed to different environmental conditions (in this case, the high-predation marine water versus the low-predation freshwater). For their article, “Relaxed Risk of Predation Drives Parallel Evolution of Stickleback Behavior”, the researchers developed a common-garden experiment in which marine and freshwater sticklebacks were tested in a lab under shared conditions to determine if their behaviors are caused by underlying genetic differences as a response to predation. Further, they also suggested that such differences have repeatedly evolved in parallel, meaning that the two separate species have produced similar characteristics but only as a result of living in similar environments, although sharing a distant common marine ancestor.

To obtain the subjects, both marine and freshwater sticklebacks were caught during their breeding season (May–June) in 8 different locations (four freshwater and four marine) in Finland and Sweden. Freshwater and marine stickleback were caught using minnow traps and a beach-seine net, respectfully. Once the fish were brought back to the laboratory, two separate aquaria were used, both consisting of two separate chambers divided by a transparent barrier. One aquarium acted as a control with no predators in the tank and another as a predation treatment that contained common marine stickleback predators (wild-caught perch). As mentioned, each tank had two sides – a behavioral arena and a holding arena. Each of the experimental trials began by transferring the stickleback fish from the holding tank into the behavioral arena of the experimental tank to run the exploration test, followed by the risk-taking test. In the exploration test, after given 3 minutes of acclimation time in a cylinder within the experimental area, the door of the cylinder was opened, allowing the fish to explore the experiment tank. During this exploratory phase, researchers recorded the latency until the head of the fish came out of the cylinder and the latency of the full body of the fish to emerge from the cylinder.

For the risk-taking test, the cylinder was removed, and fish were given 3 minutes to acclimate to the behavioral arena before food was administered to the tank. Food was provided in such a way that the fish would have to swim further and further to obtain each supplement. Hence, the more the fish ate, the further it would have to move from the refuge so that the risk experienced was equal to the reward. The measurements taken during this portion of the experiment included the time spent in the open area in the five minutes following the addition of the food item and the latency to initiate feeding after the addition of the food item. The researchers also measured the total number of feeding events as a measure of the number of successful attacks on the food item.

Figure 2 from Fraimout et al. (2022). “Behavioral variation between habitats and treatments. Mean values (circles) and standard errors (whiskered vertical bars) for the raw behavior measurements are shown for marine (blue circles) and pond (green circles) fish in the control and predation treatments. (a) Emergence time, the latency to emerge from a refuge (in seconds). (b) Feeding, the number of feeding event (count). (c) Risk‐taking, the latency to initiate feeding (in seconds). (d) Open time, the time spent in the open area (in seconds). Dashed lines represent the reaction norms for each habitat.”

The results ultimately revealed that there was a strong plastic response in most behavioral traits between both habitats in the predation treatments and that response aligned with the direction of evolutionary divergence. In this case, when exposed to predators, activity time and foraging rates decreased, while the contrary applies in opposite conditions. The study was able to successfully demonstrate that genetic differences in complex behaviors in Fennoscandian nine-spined sticklebacks have repeatedly evolved in similar environments (parallel evolution). This has most likely occurred as a response to similar selective pressures. The traits were suggested to have evolved by natural selection as well as phenotypic plasticity, contributing to the early stages of evolution in behavior in freshwater habitats.

Article: Fraimout, A., E. Päiviö, & J. Merilä. 2022. Relaxed risk of predation drives parallel evolution of stickleback behavior. Evolution 76: 2712–2723.

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