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The origin of fitness: Tracing individual fitness differences to genetic variation in a wild bird population

Final Report Summary - FITNESSGENES (The origin of fitness: Tracing individual fitness differences to genetic variation in a wild bird population)

The common buzzard (Buteo buteo) is a raptor occurring all throughout Europe and frequently observed by the public. It occurs in three distinct plumage colour morphs (types) which have been shown to differ in their lifetime reproductive success. This measure of success is called fitness and is central to our understanding of evolutionary principles. Individuals with the highest reproductive success will leave the highest number of offspring, i.e. copies of their genes, leading to the spread of these genes throughout the population over time.
Reproductive success is a complex result of genetic and environmental factors, many of which are not yet known in wild populations. However, this knowledge is needed to understand both basic evolutionary principles and how individuals, populations and species are responding to changing environments. In our project, we studied environmental effects acting on the common buzzard, and we identified the first candidate genes for differences in fitness between individuals of different plumage morphs.
The population we study is located in North Rhine-Westphalia, Germany, but individuals disperse into several neighbouring European countries. In order to track the birds over their lifetime, we mark chicks with individually labelled, clearly visible wing tags which they carry for the rest of their lives. To obtain observations on life and dead birds outside the study area, we have established a citizen science project. We inform the public on the tags and the scientific background of the research, and we ask for reports on tagged birds. The website of the project can be found at www.uni-bielefeld.de/bussarde and is available in English, German, Dutch and French. So far, over a quarter of tagged birds have been reported. Over the period supported by this grant, c. 820 chicks were tagged.
Combining reports by citizen scientists and genetic data, we were able to identify several candidate genes for buzzard behaviour. Young buzzards often leave the area of their parents’ territories during autumn or winter. This dispersal is associated with risk. We found that the timing of dispersal is strongly associated with the mean length of the genes ADCYAP1 and CREB1, as well as the colour morph of the individual.
When tagging buzzard chicks, we also obtain several other crucial types of data. To do so, nests were searched in early spring and monitored throughout the breeding season. When the chicks were 2-3 weeks old, we climbed the nest tree and brought the chicks to the ground for sampling, tagging and measurements. Small amounts of blood, feathers and saliva were taken for hormone measurements, parasite counts and genetic analyses. Further measurements included the external parasite burden, size, weight and colouration.
From the hormonal measurements, we found that stress in buzzard chicks is associated with the timing of their hatching during the season, the burden from external parasites and environmental factors such as the presence of crows and humans. However, the three colour morphs did not differ in their levels of stress hormones, suggesting that these are not associated with the differences in fitness.
In order to identify candidate genes for fitness differences, we chose to analyse the transcriptome rather than the genome of the buzzards. This subsection of the genetic material is obtained from RNA and only contains genes that are active in a specific tissue at the time of sampling. We established a uniform protocol to extract total RNA from blood, feathers, heart, muscles, brain, liver, lung and skin. However, only blood and feathers were taken from live birds. All other tissue samples came from two chicks that were found injured and taken into care but died soon after. No birds were killed for this study.
From the comparison of differently coloured feathers and other tissue, several hundred candidate genes arose. We found that many genes which are involved in the synthesis of melanin pigments, i.e. feather colouration in buzzards, differ between light and dark feathers. Furthermore, some of these genes occur in other tissues, where they could affect systems other than colouration. Most importantly, four biological pathways also involved in the regulation of stress and the immune response contain several of these genes and will therefore be of particular interest in the future.
As we have analysed the full transcriptome of the buzzard, we were able to compile an extensive database for future studies. It is the first such resource among all raptors of the large group known as Accipitriformes, i.e. most raptors except for owls and falcons. Like many wild birds, buzzards in our study population were infected with a malaria-like parasite (Leucocytozoon buteonis). These parasites live in the blood, allowing us to not only assemble the first buzzard transcriptome but also to retrieve a large percentage of the parasite’s expected genes.
The malaria-like parasites are of great interest to our study, as they may have an influence on an individual’s fitness. We found that the most successful morph (i.e. intermediately coloured individuals) mount the highest immune response, and that individuals from the least successful morph (dark) are more often infected than others. In addition, we analysed the population structure of the parasite to understand how it is spreading through the buzzard population. The pattern that emerged was slightly unusual. The parasite is not transmitted directly between buzzards but needs an insect vector to carry it from bird to bird. Still, the genetic similarity, i.e. relatedness, between parasites found in siblings was higher than expected. This was true even for siblings that hatched in different years, suggesting that they get infected by parasites that originate from their mothers. Therefore, we found first evidence of vector-borne transmission that follows the pattern which is usually expected from parasites that get transmitted directly, i.e. without an insect vector, from parents to offspring.
Our study was designed to uncover basic principles underlying fitness in a wild bird population. We have identified factors at the genetic, physiological and environmental level that have the power to influence an individual’s fitness and therefore also have the potential to affect the future population. Additionally, our work my feed into more applied research on the spread of wildlife disease. We have and are continuing to publish the results of our work in scientific papers and on the project website.