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My profession as an evolutionary biologist brings me, when not in front of a computer crunching numbers, to climb ladders and mountains in often wonderful landscapes, with the main aim of observing, capturing and ringing birds of various species. Most importantly, I undertake this repeatedly every year in the same study sites in order to maximize chances to observe the same birds, and their descendants, over time. Expressed in this way, my job description does not sound very serious or scientific. Yet in fact, the collection of data on birds in the wild, initiated by field ornithologists such as Huijbert Kluijver (1902/3-1977 — no-one, it appears, knows his true birth year) or David Lack (1910-1973) in the late 1940s has allowed in the past two decades some fundamental progress in our understanding of animal ecology and evolution. As much as I usually dread the frequent social question ‘What is the use of your research?’, I decided to contribute this piece as a tribute to the many British people who have collected data for what are probably the best informed individual-based datasets in the world. I hope to convince my readers here of the great scientific value of studies recording life-histories of birds in the long term. This will hopefully serve as a token of my appreciation for a wonderful, peaceful and productive stay in Churchill College in 2012-2013, which contributed to putting together an edited book on Quantitative Genetics in the Wild (now in press with Oxford University Press).
An individual-based monitoring in a wild population consists of marking every individual that can be captured with a unique identifier, usually a leg-ring in the case of birds, and then recording morphology, behaviour and life-history events (for example date and place of birth, age at first reproduction, reproductive events, death) until the animal can no longer be seen, or is dead. Initially, such records were used to study population dynamics and demography, using mean population estimates to understand processes such as density-dependent regulation. However, the great value of these long-term datasets currently lies in the detailed individual information which allows us to investigate the origin of variation between individuals in a host of measured characteristics. Studying this variation, and in particular disentangling its environmental and genetic origins, can contribute to answering a very diverse set of questions in evolutionary ecology. What are the causes and consequences of behavioural differences between individuals? How important are maternal effects to determine the phenotype of their offspring? (A phenotype is an observable characteristic of an organism, resulting from both genetic and environmental influences.) How are traits correlated and does that affect their potential evolution? Why do animals senesce (or age), and why is senescence rate different across individuals? How do organisms cope with brutal environmental change such as global warming? How do extravagant ornaments evolve in males?
My research as an evolutionary biologist centres on these issues. I will now consider two of the above questions and provide examples to illustrate how analysing avian long-term data can contribute to answering them.
How do organisms cope with brutal environmental change such as global warming?
One of the greatest challenges faced by mankind over the next decades is to understand and predict the consequences of global change on the world around us. The increasing human population and the expansion of its activities are causing environments to change at unprecedented rates, affecting biodiversity to such an extent that we are actually facing a sixth mass extinction. In order to mitigate these effects and allow natural populations of plants and animals to adapt, we need to contruct prospective scenarios of biodiversity trajectories. In these scenarios, populations can respond in four ways to a drastic change in the environment such as global warming: (1) they can decline and maybe become extinct; (2) individuals can disperse to a more favourable environment; (3) they can display plasticity, that is, each individual will adjust its behaviour to adjust to the new environment; or (4) the population can evolve: that is, selection pressures can lead to a change in the genetic composition of the population, thereby allowing adaptation to the novel conditions experienced. Elucidating which processes are occurring in natural populations is an essential step in predicting whether (and at what pace) these populations will adapt to the drastic global changes we are presently experiencing.
For almost a decade now, I have been working on birds of the tit family in France and the UK to address this question. Across Europe, these populations have shown a dramatic advance in their timing of reproduction. Tits have become a model species to study changes in phenology (the timing of events in an organism’s life) across their range, because they breed readily in nesting boxes, and can therefore be easily studied in a range of habitats and countries. Great tits (Parus major) studied in Wytham Woods (Oxfordshire) since 1947 have shown a fourteen-day advance in their timing of laying in the last half-century. This advance in their phenology has allowed the great tits to adjust the chicks’ food demand to the food abundance in the forest, since their main prey, caterpillars, have also shown a fourteen-day advance in phenology over the same period. In this case study, we used the long-term records on great tits to understand the origin of this phenological advance. Statistical analyses of more than 10,000 reproductive events recorded in Wytham Woods shows that the change is due to strong individual plasticity rather than evolutionary adaptation of the population. This means that each individual female has the capacity to adjust her breeding time to the phenology of the forest every year, based on cues that she collects in early spring. More recent research conducted in great tits and blue tits across different study populations of Europe shows that this plastic capacity is variable across space, and that some populations of the same species do not succeed in tracking the changes induced by global warming. Elucidating the origin of these diverse responses will contribute to predicting which populations of birds are more at risk of decline when facing climate change.
Why do animals senesce, and why is senescence rate different across individuals?
In many animal species, old individuals show a senescent decline in their reproductive performance, or an increase in their probability of dying. In some species, very old individuals even stop reproducing altogether. From an evolutionary viewpoint, senescence is difficult to explain, because natural selection favours individuals with the highest reproduction and survival capacities. Using individual records on mute swans (Cygnus olor) collected in Dorset since the late 1960s, we tested the Antagonistic Pleiotropy theory of ageing, which posits that the loss of performance in late age is a consequence of early investment in reproduction. The repeated records on the Abbotsbury birds showed that the age at first reproduction for a mute swan could vary considerably (from two to twelve years old), similarly to the age at last reproduction (from two to twenty years old). More crucially, birds that started breeding at an early age stopped reproducing earlier than the late-starters. One key aspect in this study of swans was that the long-term pedigree allowed us to show that the link between the age of start of reproduction and the age of final reproduction was actually genetic, thereby confirming a true evolutionary trade-off. Such theories are more classically tested in laboratory conditions on model species, yet these conditions can be too beneficial (for example ad libitum food) to reveal trade-offs. For this reason, it is fundamental to measure senescence in natural populations, although this is very demanding in terms of field effort over a long period.
My stay in Churchill College as an Overseas Fellow gave me the time and space to gather ideas and perspectives on our efforts in collecting data on marked individuals in wild populations of animals, and to reflect upon the immense contribution of such efforts to our understanding of fundamental processes in evolutionary ecology. This work should, as I said earlier, hopefully lead to a published book entitled Quantitative Genetics in the Wild, to be published in the spring of 2014. My gratitude goes to the whole College staff who offered me an unforgettable happy interlude in my early career.
Anne Charmantier (Originally published in the Churchill Review 2013)
Centre National de la Recherche Scientifique, Montpellier, France