Seasonal timing and population divergence: when to breed, when to migrate

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Highlights

  • Timing of reproduction and migration vary within and among populations.

  • Timing differences arise from variation in neuroendocrine mechanisms.

  • Timing differences (allochrony) can impede gene flow and thus population divergence.

  • Seasonally sympatric populations that differ in timing are excellent study systems.

  • Environmental change may act on mechanisms to influence biodiversity.

Understanding how populations adapt to constantly changing environments requires approaches drawn from integrative and evolutionary biology as well as population ecology. Timing of reproduction and migration reflect seasonal pulses in resources, are driven by day length, and are also responsive to environmental cues that change with climate. Researchers focusing on birds have discovered accelerated breeding, reductions in migration, and extensive variation in perception, transduction, and response to the environment. We consider situations in which individuals experience the same environment but differ in the timing of the annual cycle. Such scenarios provide exceptional opportunities to study mechanisms related to among-population differences in timing (allochrony) and distribution (sympatry–allopatry–heteropatry), which have the potential either to enhance or reduce population divergence and biodiversity.

Introduction

The urgency of environmental change coupled with the availability of new technology is transforming our understanding of phenomena that have fascinated biologists for generations: changing seasons, seasonal shifts in behavior and morphology, and remarkable feats of migration. The last decade has seen an explosion of studies into seasonal timing that seek to identify how changing climates are altering the biology of seasonally breeding organisms [1]. Emerging patterns in avian populations throughout the northern hemisphere include earlier breeding for many but not all species 1, 2, 3]. Migratory timing by birds has also been affected by warming 2, 4, 5, 6]. Some species have shortened their migrations or ceased migrating altogether 4, 7]. A related but distinct body of research has sought to elucidate the role of timing in phenotypic and genetic divergence among populations (see Table 1). Theoretical and empirical studies continue to challenge the view that speciation requires geographic isolation, and one focus has been to consider circumstances under which timing differences (allochrony) can give rise to reproductive isolation [8]. Studies of birds, plants, insects, fish, and bats have revealed among-population differences in timing that are interrupting gene flow, potentially leading to speciation 8, 9, 10, 11, 12].

Section snippets

Seasonal timing and population divergence

This contribution addresses how seasonality in the environment and timing of events of the annual cycle relate to population divergence by focusing on mechanisms of reproductive and migratory timing in birds. Working from the premise that selection acts on mechanisms that vary among individuals and populations and employing concepts and methods from three subfields, seasonality, evolutionary endocrinology, and geographic variation/population divergence, we briefly summarize what is new in the

Variation in timing within and among populations

It is almost a truism that members of a population experiencing the same environment will nevertheless differ among themselves in when they reproduce. Despite exposure to nearly identical day length, food supply, temperature, moisture, etc., some individuals breed early and some breed later. While some of this variation can surely be attributed to age or condition, individuals are also known to be consistently early or late owing to their underlying biological timing.

The existence of this

Timing of reproduction and migration and biodiversity

Comparisons of migrant and sedentary forms of the same species also raise the question of how migration-induced allopatry will respond to climate change and influence biodiversity. Future changes in animal movements may alter current patterns of overlap. If the tendency to migrate declines, such that currently allopatric breeding populations become sympatric, then opportunities for gene flow between migrant and sedentary forms may increase, leading to the merging of incipient species [18] and

When to breed?

Multiple reviews of selective consequences of within-population variation in timing have appeared recently 19, 20, 21]. In some cases, researchers have shown that breeding is taking place earlier in warm springs, that earlier breeding is leading to higher reproductive success, and that breeding dates are heritable. Researchers are also addressing how mechanisms of response to the environment relate to phenological change 13, 22, 23]. Nevertheless, much remains to be learned about how mechanisms

When to migrate?

Returning to our objective of how seasonality in the environment and timing of the events of the annual cycle relate to population divergence, we turn to new developments in migratory timing in birds where rapid advances are taking place owing to new technology.

Increasingly miniaturized geolocators, GPS loggers, satellite transmitters and other tracking devices deployed at breeding or wintering sites allow measurements of departure dates, migratory direction, duration and speed, and destination

Mechanisms as constraint

Reproduction and migration have traditionally been viewed as distinct stages with little to no overlap in time or neuroendocrine control mechanisms 21, 59]. However, newer findings reveal that preparation for spring migration and reproduction overlap in time and are tightly linked in mechanism 49, 50, 60]. An issue of controversy is the degree to which one life-history stage (migration) imposes a constraint on the ability of the other (reproduction) to respond independently to selection. For

Conclusion

We conclude by referring the reader to Table 1, which contains a sampling of recent studies from 13 avian systems addressing integration of timing and population divergence. Collectively these studies serve as examples of what can be learned from examining the organismal and evolutionary mechanisms that facilitate population-level divergence in reproductive and migratory timing using a range of approaches including: measurements of gene expression, endocrine correlates of reproductive and

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank the National Science Foundation [IOS-1257474 (E.D.K.) and IOS-1257527 (T.J.G)], our many talented collaborators who contributed ideas and constructive criticism, two anonymous reviewers who provided excellent suggestions for improvement, and editors Hoffman and Rubenstein.

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