Francisco Pulido

Heritability of the timing of autumn migration in a natural bird population

In recent decades, global temperature has increased at an unprecedented rate. This has been causing rapid environmental shifts that have altered the selective regimes determining the annual organization of birds. In order to assess the potential for adaptive evolution in the timing of autumn migration, we estimated heritabilities of the onset of migratory activity in a southern German blackcap (Sylvia atricapilla) population. Heritabilities (h2 = 0.34-0.45) and coefficients of additive genetic variation (CV2 = 4.7-5.7) were significant and consistent when estimated by different methods, irrespective of whether they were derived from birds hatched in the wild or bred in captivity. In an artificial selection experiment, we selected for later onset of migratory activity, simulating expected natural selection on this trait. We obtained a significant delay in the mean onset of migratory activity by more than one week after two generations of selection. Realized heritability (h2 = 0.55) was in agreement with expected heritability in the cohort that the selection line was derived from. Our results suggest that evolutionary changes in the timing of autumn migration may take place over a very short time period and will most probably be unconstrained by the lack of additive genetic variation.

Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population

Global warming is impacting biodiversity by altering the distribution, abundance, and phenology of a wide range of animal and plant species. One of the best documented responses to recent climate change is alterations in the migratory behavior of birds, but the mechanisms underlying these phenotypic adjustments are largely unknown. This knowledge is still crucial to predict whether populations of migratory birds will adapt to a rapid increase in temperature. We monitored migratory behavior in a population of blackcaps (Sylvia atricapilla) to test for evolutionary responses to recent climate change. Using a common garden experiment in time and captive breeding we demonstrated a genetic reduction in migratory activity and evolutionary change in phenotypic plasticity of migration onset. An artificial selection experiment further revealed that residency will rapidly evolve in completely migratory bird populations if selection for shorter migration distance persists. Our findings suggest that current alterations of the environment are favoring birds wintering closer to the breeding grounds and that populations of migratory birds have strongly responded to these changes in selection. The reduction of migratory activity is probably an important evolutionary process in the adaptation of migratory birds to climate change, because it reduces migration costs and facilitates the rapid adjustment to the shifts in the timing of food availability during reproduction.

Heritability of Migratory Activity in a Natural Bird Population

The presence of additive genetic variation is a prerequisite for changes in migratory behaviour through selection. Previous work with the blackcap, Sylvia atricapilla, has shown that the urge to migrate and the migratory direction are under genetic control. Here we examine whether migratory activity in this species has a significant additive genetic component, with the aim of predicting micro-evolutionary changes in migratory distance. Migratory activity was recorded in 280 southern German blackcaps from 69 families. We calculated heritabilities by parent—offspring regressions and by full-sibling correlations. Heritability estimates obtained by different methods were significantly different from zero and in good agreement with each other (h2 = 0.37—0.46). This suggests that in the expression of migratory activity maternal and dominance effects are negligible. The high amount of phenotypic and additive genetic variation found for migratory activity in this population could lead to rapid evolutionary changes of migratory habits. Under moderate selection intensities and environmental conditions similar to those presented in this study, the southern German blackcap population could evolve into a short-distance migrant in 10-20 generations.

Quantitative genetic analysis of migratory behaviour

Since the very beginning of bird migration research in the early 18th century, a number of intriguing observations have made people doubt whether migration was entirely determined by the environment. For instance, the activity of caged birds deprived of environmental cues during the migratory season, the migration of young birds without experience and without the guidance of their parents (e.g. cuckoos) and the departure from the breeding grounds in summer when conditions on the breeding grounds are still favourable could not be explained without assuming internal factors controlling these behaviours. In the 19th and early 20th century, these and other observations were explained by assuming that migratory birds possess an innate migration instinct. Until the rediscovery of Mendel’s laws and the foundation of modern genetics in the early 20th century, “genetic” research on avian migration was concerned with providing evidence for the existence of this migration instinct, and specifying which components of migratory behaviour are innate and which are acquired by experience or learning. These arguments were exclusively based on observational evidence. In the 1930s first experimental studies were conducted to explore the inheritance of migratory behaviour (e.g. Valikangas 1933; Frieling and Valikangas 1934; Nice 1934, 1937; Putzig 1938), giving birth to the field of genetics of bird migration.

Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds.

Recent climatic change is causing spring events in northern temperate regions to occur earlier in the year. As a result, migratory birds returning from tropical wintering sites may arrive too late to take full advantage of the food resources on their breeding grounds. Under these conditions, selection will favour earlier spring arrival that could be achieved by overwintering closer to the breeding grounds. However, it is unknown how daylength conditions at higher latitudes will affect the timing of life cycle stages. Here, we show in three species of Palaearctic-African migratory songbirds that a shortening of migration distance induces an advancement of springtime activities. Birds exposed to daylengths simulating migration to and wintering in southern Europe considerably advanced their spring migratory activity and testicular development. This response to the novel photoperiodic environment will enable birds wintering further north to advance spring arrival and to start breeding earlier. Thus, phenotypic flexibility in response to the photoperiod may reinforce selection for shorter migration distance if spring temperatures continue to rise.

Are Long‐Distance Migrants Constrained in Their Evolutionary Response to Environmental Change?: Causes of Variation in the Timing of Autumn Migration in a Blackcap (S. atricapilla) and Two Garden Warbler (Sylvia borin) Populations

Abstract: Long‐distance migratory birds often show little phenotypic variation in the timing of life‐history events like breeding, molt, or migration. It has been hypothesized that this could result from low levels of heritable variation. If this were true, the adaptability of long‐distance migratory birds would be limited, which would explain the vulnerability of this group of birds to environmental changes. The amount of phenotypic, environmental, and genetic variation in the onset of autumn migratory activity was assessed in two garden warbler (Sylvia borin) populations differing in breeding phenology and the length of the breeding season with the aim of investigating the effects of selection on the adaptability of long‐distance migrants. High heritabilities and additive genetic variance components for the timing of autumn migration were found in both populations. Although genetic variation in the mountain population was lower than in the lowlands, this difference was not statistically significant. Moreover, no evidence was found for reduced levels of genetic variation in the garden warbler as compared to its sister species, the blackcap (S. atricapilla). Environmental variation, however, was markedly reduced in the garden warbler, suggesting that low levels of phenotypic variation typically found in long‐distance migrants may be a consequence of environmental canalization of migratory traits. The buffering of environmental variation may be an adaptive response to strong stabilizing selection on the timing of migration. High environmental canalization of migration phenology in long‐distance migrants could potentially explain low rates of immediate phenotypic change in response to environmental change.

Proximate control and adaptive potential of protandrous migration in birds

Migration determines where, when, and in which order males and females converge for reproduction. Protandry, the earlier arrival of males relative to females at the site of reproduction, is a widespread phenomenon found in many migratory organisms. Detailed knowledge of the determinants of protandry is becoming increasingly important for predicting how migratory species and populations will respond to rapid phenological shifts caused by climatic change. Here, we review and discuss the potential mechanisms underlying protandrous migration in birds, focusing on evidence from passerine species. Latitudinal segregation during the non-breeding period and differences in the initiation of spring migration are probably the key determinants of protandrous arrival at the breeding sites, while sexual differences in speed of migration appear to play a minor role. Experimental evidence suggests that differences between the sexes in the onset of spring migratory activity are caused by differences in circannual rhythmicity or by photoperiodic responsiveness. Both of these mechanisms are hardwired and could prevent individuals from responding plastically to chronic changes in temperature at the breeding grounds. As a consequence, adaptive changes in both the timing of arrival in spring and of reproduction will require evolutionary (genetic) changes of the cue-response systems underlying the initiation and extent of migration in both males and females.

Correlation between timing of juvenile moult and onset of migration in the blackcap, Sylvia atricapilla

Abstract In small bird species, energy-demanding life cycle stages such as moult and migration are generally separated in time. The extent of separation can vary considerably within and between species, but the causes of this variation are largely unknown. We studied the phase relation between postjuvenile moult and autumn migration by experimentally manipulating the timing of these events in the blackcap. In a split-brood experiment, we hand-reared 30 blackcaps and kept them under either natural daylengths or a time-shifted photoperiod that altered the timing and intensity of moult. We determined the onset and termination of moult and the onset of nocturnal migratory restlessness. In both groups, onset of migratory activity was correlated with termination of moult. The extent of moult–migration overlap was unaffected by the photoperiod manipulation, suggesting resilience of this correlation against environmental perturbation. Strong family effects explained a large proportion of phenotypic variation. The correlation between the timing of postjuvenile moult and migration is, therefore, likely to result from genetic covariation. We predict that selection for delayed termination of moult will result in more overlap between moult and migration. Because of this correlated selection response, adaptive changes in the timing of migration could be retarded, and independent adaptive evolution of moult and migration schedules could be constrained.