Genetic Basis and Evolutionary Aspects of Bird Migration

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Bird migration is a phenomenon of superlatives in terms of multitudes, distances, physiological adaptations, and orientation performance. Opinions concerning the origin of bird migration differ widely. The chapter summarizes the theories related to evolution of bird migration. Birds possess the circannual rhythms such as endogenous annual cycles and internal calendars as special forms of biological clocks. The physiological body rhythms control the course of many events with annual periodicity in a multitude of different animals from coelenterates to mammals, and in plants. Migratory restlessness (Zugunruhe), the nocturnal activity of normally diurnally active but night-migrating species represents an inherited population-specific program for migration and thus is a reliable instrument for studying migratory birds in captivity. Systematic investigations of many aspects—migratory behavior (activity), date of departure, migratory direction, termination of migration and goal finding, juvenile development, migratory disposition, and prerequisites as well as partial migration demonstrated strong genetic influence. Inheritance now appears to be a basic component of the control of bird migration. The genetic studies showed that partial migration enhances the understanding of the control and adaptability of migratory behavior, and helps to develop a new theory concerning the evolution of bird migration. The chapter discusses a new theory of the evolution, control, and adaptability of avian migration. The new theory predicts that when environmental conditions are changing rapidly, the migratory behavior of bird species should adapt with appropriate microevolutionary speed. Thus, based on the new results on genetic control and the extremely high potential for evolutionary change in regards to bird migration, some predictions are made in relation to further global warming effects that may result in major restructuring of entire avifaunas.

Introduction

Bird migration is a phenomenon of superlatives, intensely interesting to humanity for millennia and probably since primeval times. With about 50 billion individuals migrating every year along a network of routes that encompass the entire earth, bird migration is observable universally throughout the year. People in practically every geographical region are constantly in contact with it, and most will eventually consider the questions that are at the core of migratory scientific research (Berthold, 2001). To begin with, why do birds migrate at all, and given that they do, why do they travel such vast distances? Some of them cover 30,000 to 50,000 km annually, or approximately the circumference of our planet, and non-stop flights may be as long as 7,500 km. How do they manage this? How can they cross oceans and deserts in relative safety and fly over mountains as high as 10,000 m without suffering altitude sickness? There are partially migratory populations, with some members that spend the winter abroad while others remain in the breeding grounds—what determines who goes and who stays? What tells the migrants when to depart and when the journey is over, and what keeps the migration in progress for a few hours in some cases but for more than half a year in others? How can migratory birds orient themselves so precisely over thousands of kilometers—for instance, on a journey between their nest in a farmer's barn within the breeding area and a particular branch on a tropical tree for roosting while in the winter quarters—with pinpoint navigation sharp enough to locate both destinations every year? Furthermore, what enables their amazing temporal precision every year, sufficient for many of them to schedule the migration almost down to the day, so that one could set the calendar by them (indeed, these have been called “calendar birds”)? Now there is something new to ask: What makes them able to adjust so rapidly to the changes in environmental conditions currently being caused by global warming? This ability is especially astonishing in the case of the many songbird species, most of which have their migratory experience limited to their lifetimes (a little over a year) and nevertheless behave as the times demand.

Bird migration is superlative not only in terms of multitudes, distances, physiological adaptations, orientation performance, and the like, but has also been extraordinarily well-studied. The reason is that birds are the most attractive group of organisms we know. No other animal has captivated so many enthusiasts and especially amateur researchers worldwide—in the USA and Europe alone they now number in the millions. The attractions of these animals are obvious: appealing body shape, colorful plumage, conspicuous and sometimes beautiful song, graceful movements—especially in flight—as well as many other aspects of their behavior and ubiquitous presence. Not only do we know them as constant companions in our settlements, but we also encounter them regularly on our travels to remote deserts, mountains, and fields of arctic ice. The result of all this is that ornithology has become a unique “scientia amabilis,” such that over the centuries migration has been more thoroughly studied than almost any other natural phenomenon. This has had two main outcomes. On one hand, an unequalled database of migratory information has been created, extending far back into the past. This enables us to rapidly recognize changes when they occur—for example, a later-than-usual onset of migration, or the adoption of new winter quarters. On the other hand, we are now faced with an abundance of hypotheses and theories, especially about the evolution of migration, its controlling mechanisms, and the orientation of migrating birds. Some of these have propelled the research forward, but others have held it back. The emphasis on experimental studies in the last three decades or so has brought decisive advances in many areas, such as in our understanding of how migration is grounded in genetics and evolution. The following overview is concerned mainly with these two aspects of biology.

Section snippets

The Broad Palette of Theories on Control Mechanisms and Evolution

Today those who study bird migration largely agree that the main reason for undertaking a migratory journey is ultimately related to feeding conditions. However, these conditions affect the birds in two distinct ways. One is that a sudden, temporary lack of food causes the birds to leave, such as in the case of insectivorous species at the higher latitudes. Secondly, the birds seek out regions in which at certain seasons the food supply is particularly abundant and other conditions are

The Discovery of Circannual Rhythms: The Challenge to Genetic Studies

As long ago as 1702, von Pernau surmised that bird species at higher latitudes that begin their outward migration very early in the year—for instance, in July⧸August—are not simply “driven away by hunger and cold,” but rather there is “a hidden drive forcing them [to depart] at the right time,” which often proves to be when the summer half-year is at its peak. Nevertheless, it took until the 1960s for ideas about endogenous control of bird migration (and also about annual periodicity of

The Search for and Selection of Bird Species Suitable for Testing

At an early stage, in the “warbler program” set up in our institute (e.g., Berthold et al., 1970) to investigate the biology of one bird group as comprehensively as possible, it had come to our attention that the blackcap (Sylvia atricapilla) was an outstandingly suitable candidate. Of the diverse forms of migratory behavior known to exist in the Eurasian-African system of migratory birds, the various widely-distributed populations of blackcaps exhibit more than any other species (Figure 2). In

The Approach

In an initial experiment (1978 and 1979) we succeeded in demonstrating, by crossing blackcaps from Africa (Canary Islands, partial migrants) and Europe (southern Germany, exclusive migrants), that the population-specific time program of migratory activity is inherited (genetically controlled; Berthold and Querner, 1981). The results also provided strong evidence that the migratory behavior (the “migratory drive” of the former literature) as well as morphological features and juvenile

Mode of Inheritance

The first person to devote close attention to the question of whether migratory behavior is inherited was Nice, beginning in 1933. Studying the song sparrow, she constructed genealogies in an attempt to find out whether these partially migratory birds pass migratory activity on to their descendants, as a “migration instinct.” Failing to find any pure strains of migrants or of residents, and instead discovering that parents showing migratory activity can also produce nonmigratory offspring and

The Distribution and Key Role of Partial Migration

As expected (Section V.H), our genetic studies showed partial migration to be very informative, enhancing our understanding of the control and adaptability of migratory behavior as well as helping us to develop a new theory concerning the evolution of bird migration. Since partial migration had been revealed as a kind of turntable between migratory and sedentary behavior, we wondered how widespread partial migration is, and where transitions from migrating to not migrating might be possible. In

A New Theory of the Evolution, Control, and Adaptability of Avian Migration

The new results on genetic control of bird migration, obtained mainly with blackcaps and redstarts, along with the recent information about how partial migration is controlled, leads quite inevitably to a novel, simple, and yet comprehensive theory of bird migration. It will be presented in five core statements.

  • 1.

    Birds evolved migratory behavior very early, close to their origin in both space and time.

  • 2.

    Like the birds themselves, their migratory behavior evolved in tropical regions, or at least

Observations so far

One of the predictions of the new bird migration theory, introduced in Section VIII, is that when environmental conditions are changing rapidly, the migratory behavior of bird species should adapt with appropriate microevolutionary speed. This is just what we are seeing now, and have been observing for some time, as global warming has set in. Some of these changes are so pronounced that, even if we knew nothing about the current climatic warming, we would be forced to conclude that some

Outlook

At present the world is characterized by a general decline in biodiversity, and the birds of interest here are no exception; at least at higher latitudes, migratory birds are relatively severely affected. On the other hand, as described in the preceding sections, it has become clear that migratory birds in particular are strongly influenced by their genetic construction in terms of their complex behavior and physiology. Since large proportions of phenotypic variation within populations are

Summary

Bird migration, a phenomenon of superlatives involving the most attractive group of organisms, has received so much attention that this area of research now provides an unequalled database as well as an abundance of hypotheses and theories concerning evolution, control, and orientation. The discovery of circannual (endogenous annual) rhythms in the 1960s has stimulated a new research field: experimental genetics of avian migration, soon followed by experimental evolutionary studies. Pilot

Acknowledgements

The long-term studies on blackcaps that have allowed us to establish the genetic basis and evolutionary aspects of bird migration were made possible by the continuous support given us by the Max Planck Society and the German Research Foundation (Deutsche Forschungsgemeinschaft). But the crucial factor for ultimate success has been the collaboration with Ulrich Querner since 1969, Gabriele Mohr since 1978 and Francisco Pulido since 1984; together we formed the “hard core” of a larger team,

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