The potential consequences of unintended artificial selection on population fitness

The human factor on natural selection Artificial selection can be unintended, where human activities have affected wild populations in ways that were not foreseen. Professor Claus Wedekind and his colleagues are investigating whether natural populations of salmonids have the evolutionary potential to adapt to the presence of different stressors in their environment.

Artificial selection has long been used by humans to breed crops and animals like cows, sheep and fish with specific traits that will then be passed on to the next generation, traits which may make them more attractive to consumers. Alongside intended artificial selection, there are also cases of unintended artificial selection, where human activities have affected wild populations in ways that were not anticipated. “For example, there is selection by pollution or climate change, or by non-random harvesting. Lots of human activities can create new forms of selection on natural populations,” explains Claus Wedekind, a Professor in the Department of Ecology and Evolution at the University of Lausanne. In his research, Professor Wedekind is studying the evolution of natural populations in today’s environments, which are very much influenced by human activities.

“If human activities lead to pollution in a river for example, and the fish in this river have genetically-based differences in their tolerance towards the pollution, then we predict that the pollution will change the allele frequencies in that fish population over time,” he outlines.

Allele frequency This will lead to evolution, which can be broadly summarised as change in allele frequency over time, a topic which lies at Freshly caught whitefish (Coregonus suidteri).

the heart of Professor Wedekind’s work as the lead of an SNF-funded research project.

One question that Professor Wedekind and his colleagues in the project are studying is whether a given population of fish has the potential to adapt to a changing environment.

“We study fish in Switzerland which belong to the salmonid family, such as grayling and brown trout,” he says. This work involves studying natural populations of fish through a combination of field observations and laboratory experiments, with the aim of building a fuller picture of how they are

The aim here is to expose the fish to certain things that have been identified as relevant, such as the drugs that are regularly found in streams and rivers in Switzerland. One prominent example is ethinylestradiol, a synthetic oestrogen that’s used in contraceptive pills and is known to be toxic to fish; it cannot be broken down by wastewater treatment plants so it can seep into ecosystems. “Ethinylestradiol is a stressor, a pollutant that has been around for sixty years – and here we can test whether we see signs of adaptation to it in certain fish populations,” outlines Professor Wedekind.

We want to see whether the change in allele frequencies can be somehow linked to the level stressors. This is about quantitative genetics. changing. “We sample breeding fish from the wild, so males and females from the spawning location. We measure their phenotypes and take a tissue sample to study their genetics then we use their gametes - their eggs and sperm - for in vitro fertilization.

It’s fairly easy to collect eggs and sperm,” explains Professor Wedekind. “Then we do experimental breeding. We take a sample of these families, bring them to the laboratory, and test them for their stress tolerance under very controlled experimental conditions.”

Setting the gill nets.

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The fish are exposed to ecologically relevant concentrations of ethinylestradiol and other drugs, essentially replicating natural conditions in the laboratory. “We consider everything that we believe could be ecologically relevant, such as changes in temperature. We test these factors in the laboratory on a sub-set of the family at concentrations or levels that have this ecological relevance,” continues Professor Wedekind. “The rest of the family is raised by wildlife managers in hatcheries, and then released into the wild at different stages.”

Juvenile brown trout (Salmo trutta).

This typically happens when the fish are very young larvae, then they are subsequently monitored. If they are caught by fishermen in the wild later on in their lives, their genetic background can be reconstructed. “When we take a tissue sample of a fish, we can assign the fish to its mother and father using DNA fingerprinting,” explains Professor Wedekind. In the course of the project around half a million brown trout and half a million grayling have been released, and while the majority will die, some will survive and be caught, from which Professor Wedekind hopes to gain fresh insights. “With the genetic assignment, we can ask which father and which mother has the most reproductive success under the situation they face. How successful are they? Then we can link that to the stress tolerance that we’ve measured in the laboratory - we can test whether what we measured in the lab accurately represents what happens in nature,” he says. “We want to see whether the change in allele frequencies can be somehow linked to the level of stressors. This is about quantitative genetics.”

Evolutionary potential The primary focus here is to see whether populations have the evolutionary potential to adapt to the presence of various stressors. The toxicity of ethinylestradiol has been measured in the laboratory, and it has been found that even very small amounts have detrimental effects.

“We exposed an embryo to just a picogram (10-12 of a gram) of ethinylestradiol and we could see that this reduced growth. It didn’t kill the embryo, but it reduced growth,” outlines Professor Wedekind. The concentrations of this toxin are highest close to wastewater treatment plants, an issue that Professor Wedekind has taken into account in his research. “We’ve compared fish populations that live close to Adult brown trout in the photo box.

Stripping eggs from a brown trout.

wastewater treatment plants to fish populations that live in lakes and are not really exposed to ethinylestradiol at all,” he explains. “We would predict that if populations have adapted to this stressor, then those fish that live closest to wastewater treatment plants would have become better at dealing with the toxicity. We would not expect fish that live further away to have evolved a tolerance to ethinylestradiol.”

Evidence gathered so far in the project supports this hypothesis, with Professor Wedekind and his colleagues testing predictions based on several different evolution scenarios. River-dwelling fish such as grayling and brown trout show a higher tolerance to ethinylestradiol than lakedwelling species like lake char and different whitefish species that are not exposed to the same extent. “We also find that there is genetic variations in tolerance in these populations that are not exposed to the stressor,” says Professor Wedekind. Genetic variation has not been found in river-dwelling fish, which means that at the moment these populations don’t have the potential to adapt to ethylinstradiol. “We believe that they had that potential in the past, but it has been lost over the last six decades, although we need more data to prove that,” continues Preparing a full-factorial breeding experiment, with eggs (orange mass) of 5 females and sperm (white drops) of 5 males in all 25 possible combinations. Addition of water will activate the sperm and fertilisation will happen.

Sampling fin tissue for later genotyping.

Professor Wedekind. “At the moment we predict that in river-dwelling fish, you would not see genetic variation for tolerance to ethylinstradiol because evolution has happened and used up the genetic variation.”

The data gathered in the project could be used to quantitatively estimate the key parameters of evolutionary models, which would then enable scientists to produce quantitative estimates of future scenarios. The main intention with this research is to build a deeper understanding of how natural populations are changing, yet Professor Wedekind says it also holds relevance for wildlife managers. “We’re doing basic research, to produce knowledge for the textbooks of the future on the one hand, but also to support wildlife management,” he outlines. Salmonids are typically keystone species that largely define the ecosystems they inhabit, while they also The last juvenile brown trout of many that were sampled from the wild.

Lake Hallwil and the Swiss Alps.

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The potential consequences The potential consequences of unintended artificial selection on population fitness: combining laboratory experiments with large-scale field studies on salmonids

Project Objectives

The project combines observations (mostly long-term monitoring) with molecular genetics, modelling, and experimental research on various salmonid fish. The main aim is to better understand unintended artificial selection (e.g. by size-selective fishing, pollution, and changed natural and sexual selection in supportive breeding) and how it influences the evolution and the long-term survival of wild populations.

Project Funding

The project is funded by the Swiss National Science Foundation, with additional support from the Aargau Lottery Fond.

Project Partners

The project profits from collaborations with many other laboratories and is a close collaboration with various cantons, especially Bern and Aargau, several fishing organizations, and professional fishermen.

Contact Details

Project Coordinator, Claus Wedekind Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland.

T: +41 21 692 42 50 E: claus.wedekind@unil.ch W: https://www.unil.ch/dee/wedekind-group Claus Wedekind

Claus Wedekind is an evolutionary ecologist with strong interests in sexual selection, conservation, and cooperation among unrelated individuals. He did his Ph.D in 1994 at the University of Bern, and later worked as research fellow or lecturer at the Universities of Bern, Edinburgh, Utah, Harvard, Zürich, and the EAWAGETH, and has been professor at the University of Lausanne since 2006.

hold wider significance. “They are typically quite economically important, because anglers and fishermen target them. They are also culturally important – there is a lot of concern about the decline of many of these populations,” explains Professor Wedekind. “So we get lots of support from the Swiss cantons. They collaborate with us and want to understand what is happening to their populations, and what could be done to halt the decline.”

Sexual selection A further topic that Professor Wedekind is addressing in his research is the potential of sexual selection for population fitness. In many wild species, parents compete for access to mating partners; however, large numbers of fish are produced in hatcheries and therefore have parents that did not choose each other, now Professor Wedekind is looking into the consequences of this. “Should we worry about the genetics of the next generation that has been produced by this random mating?” he asks. With random mating, the offspring survival rate in a laboratory experiment under given stressor conditions was shown to be about 85 percent, but this increased when the female had the opportunity to choose between different males. “If we assume that the female always knows which male would be best for her offspring, then giving them the choice between two males would increase offspring survival rates by 5 percent points, which means mortality would decrease by one third (from 15% to 10%),” outlines Professor Wedekind.

A pattern emerges that the more males the females could choose from, the higher the potential benefit of their choice. The question then arises of whether females are able to identify the best males; one signal of genetic quality in whitefish is the strength of their A whitefish prepared for morphometry.

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tubercles, little structures on the skin. “Tubercles are only developed for the breeding season, and after it they immediately fall off. Males differ in the strength of these tubercles,” says Professor Wedekind. The use of a 3D scanner enables his team to measure the volume of these tubercles, and that can then be linked to offspring survival rates. “It might be expected that males with larger tubercles are genetically better, and that females would pick them. We have found a lot of evidence that this is indeed the case but it’s more complicated than that,” he continues. “We’ve also seen evidence of different male strategies in signalling – some males seem to signal very honestly and others don’t. Nevertheless, there is a clear potential for breeding tubercles to signal genetic quality.”

These are just a few of the questions that Professor Wedekind is investigating, with research ongoing into a number of different areas, including adaptation to climate change and the evolutionary consequences of exploitation. While much of this research has been conducted on salmonids, Professor Wedekind says it holds relevance to wild populations more generally. “We are using the salmonids as a model to study general questions about evolution and population management.

If you can demonstrate in one population that by allowing females to choose males, you would increase offspring survival, then you have good reason to believe that the principle could be relevant for many other species,” he says. The project’s findings on sexual selection also have wider implications. “We have sexual selection in plants and I think there’s no example of a species without any form of sexual selection. So by studying the potential of sexual selection in one species, we learn a lot about the potential of sexual selection in general,” concludes Professor Wedekind.

The field lab on a winter morning.

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