Timothy Coppack

Predicting life-cycle adaptation of migratory birds to global climate change

Analyses of long-term data indicate that human-caused climatic changes are affecting bird phenology in directions consistent with theoretical predictions. Here, we report on recent trends in the timing of spring arrival and egg laying found within a western European Pied Flycatcher Ficedula hypoleuca population. Mean egg laying date has advanced over the past 20 years in this population. The advancement in egg laying date was stronger than the advancement of spring arrival, suggesting that Pied Flycatchers are changing these stages of their annual cycle at different rates. It could be shown that selection for earlier breeding had increased. Hence, the observed adjustment in laying date did not match the advancement of spring. Our findings raise general questions about the adaptability of migratory birds to rapid environmental changes. Adaptive advancement of reproduction in response to increasing spring temperatures and to the concomitant advancement of food supply could be held back, because annual breeding and migration cycles are controlled primarily by endogenous rhythms and photoperiodic cues which do not relate to temperature. Migrants may have several options for arriving earlier on the breeding grounds, including an increase in migration speed, earlier departure from the wintering area or a shortening of migration distance. Changes in migratory behaviour could be accomplished either by phenotypic plasticity or by selection on different genotypes. Although descriptive field data provide compelling evidence for changes in, and possible constraints on, the timing of breeding and migration, their explanatory power in predicting the limits of adaptation remains restricted. We review recent experimental approaches, which explicitly test the relative roles of genetic versus environmental factors in the adaptation of life-cycle timing to global environmental changes.

A framework for the study of genetic variation in migratory behaviour

Evolutionary change results from selection acting on genetic variation. For migration to be successful, many different aspects of an animal’s physiology and behaviour need to function in a co-coordinated way. Changes in one migratory trait are therefore likely to be accompanied by changes in other migratory and life-history traits. At present, we have some knowledge of the pressures that operate at the various stages of migration, but we know very little about the extent of genetic variation in various aspects of the migratory syndrome. As a consequence, our ability to predict which species is capable of what kind of evolutionary change, and at which rate, is limited. Here, we review how our evolutionary understanding of migration may benefit from taking a quantitative-genetic approach and present a framework for studying the causes of phenotypic variation. We review past research, that has mainly studied single migratory traits in captive birds, and discuss how this work could be extended to study genetic variation in the wild and to account for genetic correlations and correlated selection. In the future, reaction-norm approaches may become very important, as they allow the study of genetic and environmental effects on phenotypic expression within a single framework, as well as of their interactions. We advocate making more use of repeated measurements on single individuals to study the causes of among-individual variation in the wild, as they are easier to obtain than data on relatives and can provide valuable information for identifying and selecting traits. This approach will be particularly informative if it involves systematic testing of individuals under different environmental conditions. We propose extending this research agenda by using optimality models to predict levels of variation and covariation among traits and constraints. This may help us to select traits in which we might expect genetic variation, and to identify the most informative environmental axes. We also recommend an expansion of the passerine model, as this model does not apply to birds, like geese, where cultural transmission of spatio-temporal information is an important determinant of migration patterns and their variation.

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.

Degree of protandry reflects level of extrapair paternity in migratory songbirds

Males of most migratory organisms, including many birds, precede female conspecifics on their journey to the breeding areas. Several hypotheses have been proposed to explain the evolution of protandrous migration, yet they have rarely been tested at the interspecific level. Here, we provide correlational support for the “mate opportunity” hypothesis, which assumes that selection favours protandry in polygynous species where males gain significant fitness benefits from arriving earlier than females. Drawing on phenological data collected at two northern European stopover sites, we show that the time-lag in spring passage between males and females of five Palearctic migratory songbird species is positively associated with levels of extrapair paternity available from the literature. This suggests that males arrive relatively more in advance of females in species with high sperm competition where sexual selection through female choice is intense. Thus, protandry may arise from selection on the relative arrival timing of males and females rather than from selection within one of the sexes.

Weather and fuel reserves determine departure and flight decisions in passerines migrating across the Baltic Sea

Departure decisions of how and when to leave a stopover site may be of critical importance for the migration performance of birds. We used an automated radiotelemetry system at Falsterbo peninsula, Sweden, to study stopover behaviour and route choice in free-flying passerines departing on flights across the Baltic Sea during autumn migration. In addition, we had an offshore receiver station (FINO 2) located about 50 km southeast from Falsterbo. Of 91 birds equipped with radiotransmitters, 19 passed FINO 2. The probability that a departing migrant passed near FINO 2 was primarily affected by winds and timing of departure. Probably, the migrants were subjected to drift by westerly winds, leading to southeasterly flight paths and an enhanced probability of passing FINO 2. Most birds passing the offshore station departed early in the night, which indicates that southward departures across the Baltic Sea usually take place during this time window. Wind condition was the dominant factor explaining the variation in flight duration between Falsterbo and FINO 2. After considering wind influence, we found additional effects of fat score and cloud cover. Birds with a higher fat score performed the flight faster than leaner individuals, as did birds that departed under clear skies compared to birds departing during overcast skies. These effects may reflect a difference in migratory motivation and airspeed between lean and fat birds together with difficulties in controlling orientation in overcast situations on oversea flights when celestial cues are unavailable. Thus, winds, clouds and fuel reserves were the primary factors determining departure and flight decisions in passerine migrants at Falsterbo in autumn

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.

Adaptive hypotheses for protandry in arrival to breeding areas: a review of models and empirical tests

Our understanding of avian migration has progressed significantly, yet the selective conditions that favor the arrival of males before females at the site of reproduction remain largely unclear. Here, we review the leading adaptive hypotheses for protandry, highlight some key empirical studies that test protandry theory, and identify theoretical and empirical information demands. In general, protandry should evolve in species where the variance in male reproductive success is larger than in females if the costs to males of earlier arrival relative to calendar date (viability selection) can be balanced by increased mating opportunities (sexual selection). Early arrival by males can provide ‘priority benefits’ that help in the monopolization of resources or ‘early bird draw benefits’ that increase opportunities for extra-pair mating. While some empirical studies are consistent with theoretical predictions regarding the important selection factors that influence protandry (e.g., extrinsic mortality and extra-pair paternity), some are not, and some studies focus on ecological factors that have not been considered explicitly by theory. We call for an integrated theoretical approach to help formalize how protandry should evolve in response to the antagonistic roles of natural and sexual selection, the nature of competitive asymmetries among males or females, sex-specific costs and benefits of early arrival, and various climate change scenarios.

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.

Circadian flight schedules in night-migrating birds caught on migration

Many species of migratory birds migrate in a series of solitary nocturnal flights. Between flights, they stop to rest and refuel for the next segment of their journey. The mechanism controlling this behaviour has long remained elusive. Here, we show that wild-caught migratory redstarts (Phoenicurus phoenicurus) are consistent in their flight scheduling. An advanced videographic system enabled us to determine the precise timing of flight activity in redstarts caught at a northern European stopover site during their return trip from Africa. Birds were held captive for three days in the absence of photoperiodic cues (constant dim light) and under permanent food availability. Despite the absence of external temporal cues, birds showed clear bimodal activity patterns: intense nocturnal activity alternating with diurnal foraging and resting periods. The onset of their migratory activity coincided with the time of local sunset and was individually consistent on consecutive nights. The data demonstrate that night-migrating birds are driven by autonomous circadian clocks entrained by sunset cues. This timekeeping system is probably the key factor in the overall control of nocturnal songbird migration.

Experimental determination of the photoperiodic basis for geographic variation in avian seasonality

Geographic variation in the timing of breeding, moult and migration of birds reflects adjustment of their annual cycles to regional differences in environmental conditions. Understanding to what degree this variation results from phenotypic plasticity or from genetic adaptation is important both as a goal of primary research and especially because we need to understand the potential for species to adapt to global environmental change. The annual change in day-length remains invariant, year after year, and birds depend primarily on this environmental information to match breeding and migration schedules with the changing seasons. Here, I review what is known about the role of photoperiodic responses in shaping geographic variation in avian life cycles, focussing on intraspecific comparative studies in passerine birds. Experiments with hand-raised individuals from different populations kept under identical conditions (common-garden experiments) suggest that differences in the timing of events are not photoperiodically determined when trait differences persist. A single common-garden experiment has no neutral testing ground, however. Thus, if birds breeding at different latitudes have evolved (or retained) non-parallel reaction norms, a single test environment is not sufficient to quantify genetic and environmental influences. While reciprocal transplantation may control for this problem, such an extended experimental design has only rarely been considered. More recently, population-specific reaction norms have been studied by assigning full siblings to various photoperiodic regimes. Through this approach, the extent of genotype-by-environment interaction can be estimated, which is essential information when interpreting trait differences among populations under natural conditions and predicting how species or populations will respond to photoperiodic conditions outside present-day geographical ranges.