Bart Kempenaers Talks About Darwinian Fitness in Natural Populations

New Hot Paper Commentary, May 2011

Bart Kempenaers

Article: Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations

Authors: Korsten, P, et al.
Journal: MOL ECOL
Volume: 19, Issue: 4, Page: 832-843, Year: FEB 2010
* Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, Seewiesen, Germany.
* Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, Seewiesen, Germany.
(Addresses have been truncated)

Bart Kempenaers talks with and answers a few questions about this month's New Hot Paper in the field of Environment & Ecology.

SW: Why do you think your paper is highly cited?

The paper presents the first between-population comparison of an association between genetic variants of a dopamine receptor gene (DRD4) and variation in exploration of a novel environment, which has been related to differences in "personality," in a wild animal, the great tit (a common European songbird). The study was the result of a large-scale and successful collaboration between researchers from several European research institutes, including the Max Planck Institute for Ornithology (Germany), the Netherlands Institute of Ecology, and the Universities of Groningen (The Netherlands), Antwerp (Belgium) and Oxford (UK).

Our paper quickly caught the attention of researchers who are studying the evolution of personality variation, also in humans, and of researchers who are investigating the evolutionary genetics of wild animal populations and who are searching for genetic variants that explain variation in Darwinian fitness in natural populations. Today, the research fields of both the evolution of personality variation and the evolutionary genetics of wild animal populations are quickly expanding.

SW: Does it describe a new discovery, methodology, or synthesis of knowledge?

Our paper confirms the presence of an association between the dopamine receptor gene and exploratory behavior previously found in a single great tit population in the Netherlands. However, our study also shows that this association is weaker or is even absent in three other European great tit populations, in Belgium, the UK, and another population in the Netherlands. Our finding of these differences between populations highlights that we should interpret the results of genetic association studies, also in humans, with great care.

SW: Would you summarize the significance of your paper in layman's terms?

"Our research is rather fundamental, but ultimately, this research on the ecological and evolutionary genetics of natural animal populations will help us understand how genetic variation for behavioural and ecological characteristics is maintained in the wild."

Our research identified a gene (called "DRD4" and coding for a receptor protein that plays a role in signal transduction in the central nervous system) that may cause differences between individual wild birds in how they deal with new situations. This is important because it will allow us to study how such individual differences evolve and are maintained under the influence of natural selection in the wild. This will help us to understand why such a huge variation in personality among individuals has evolved in humans.

Our study also showed that the DRD4 gene was not consistently related to the birds' behavior when different wild populations of birds across Europe were compared. This indicates that we should be very careful in drawing quick conclusions from genetic studies on single populations. It is crucial to repeat the same studies in different populations to test the generality and robustness of the initial findings. This note of caution also applies to studies of genetic associations in humans, for example studies that investigate genetic risk factors for disease.

SW: How did you become involved in this research, and how would you describe the particular challenges, setbacks, and successes that you've encountered along the way?

Our work on the link between DRD4 gene variants and avian "personality" started in 2003, at one of our group's daily 10.00h coffee breaks. At the time, Dr. Andrew Fidler—a molecular geneticist now at the Cawthron Institute in Nelson, New Zealand—worked at the Max Planck Institute for Ornithology in Seewiesen. We discussed the emerging possibilities to use information from work on the human genome for linking genetic variants to individual variation in behavior of free-living birds.

At the Netherlands Institute of Ecology in Heteren, Dr. Piet Drent and his colleagues, in particular Dr. Kees van Oers, had obtained data on individual variation in exploratory behavior in captive great tits and they found that part of this variation was heritable. Andrew told us that variants of the DRD4 gene had been linked to aspects of human personality, in particular to individual variation in novelty-seeking behavior, and suggested to investigate whether something similar could be going on in birds. That's when the project was born.

The first challenge at the time was to identify the DRD4 gene in the great tit, and to sequence it. Our lab technician Sylvia Kuhn spent a lot of time and effort on this, but when she finally succeeded, and once the potentially relevant gene variants were identified, the genotyping of individuals went fast.

A second challenge was to initiate the collaboration with the people in Heteren. They had all the hard-won behavioral data and they were a little surprised by our question whether we could make use of their data and their blood samples for DNA extraction, because we did not have much to show them in terms of previous experience with the candidate gene approach. During meetings in Heteren and Seewiesen, we all soon agreed that DRD4 genotyping of birds with known exploration data would be a worthwhile enterprise and to give it a go. That's how the first paper on the DRD4 gene in great tits came about (Fidler et al. 2007, Proc. R. Soc. B).

This paper triggered the next project: several labs in Europe were collecting standardized data on exploratory behavior of wild great tits, so we contacted our colleagues and they all immediately agreed to send us DNA samples for analysis. It was a great pleasure to work with all of them and a fantastic opportunity to use such an extensive dataset on individual variation in behavior of free-living birds.

Thanks to the hard work of many behavioral ecologists collecting these data, we could repeat our analysis in the original population where we first found the link between DRD4 and exploratory behavior, and in three additional populations. Dr. Jakob Mueller and Dr. Peter Korsten, who was awarded an Alexander von Humboldt fellowship to join the research project, played an important role in the DRD4 genotyping and final analyses of the associations between the variants of the DRD4 gene and individual variation exploration behavior in the different great tit populations.

SW: Where do you see your research leading in the future?

We will identify more genetic variants that are related to functional behaviors and consequently have effects on Darwinian fitness in wild animals. For example, recently we identified a gene of which different variants relate to differences in migratory behavior in a wild songbird, the blackcap, which flies from its breeding grounds in Europe to Southern Europe, to the British Isles or Africa for overwintering.

The identification of genetic loci that influence functional behaviors in wild animals will hopefully allow us to investigate how frequency changes of genetic variants over time underpin the micro-evolutionary process in natural populations, for example resulting in evolutionary adaptation to environmental change.

SW: Do you foresee any social or political implications for your research?

Our research is rather fundamental, but ultimately, this research on the ecological and evolutionary genetics of natural animal populations will help us understand how genetic variation for behavioral and ecological characteristics is maintained in the wild. The maintenance of such genetic variation in the face of continual natural selection is one of the great puzzles of evolutionary biology and the occurrence of such variation determines the potential of wild populations to adapt to changes in their natural environment, for example due to habitat fragmentation and climate change.End

Prof. Dr. Bart Kempenaers
Department Behavioural Ecology & Evolutionary Genetics
Max Planck Institute for Ornithology
Seewiesen, Germany



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