Seasonal timing and population divergence: when to breed, when to migrate
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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2018, Journal of Theoretical BiologyCitation Excerpt :There has been a lack of attention to how seasonality might affect host evolution in theoretical studies, even though it has been shown that epidemiological dynamics can be greatly impacted by a variable environment (Altizer et al., 2006; Grassly and Fraser, 2006). In addition, it is well known that a wide range of species reproduce seasonally due to environmental fluctuations, for example in bats (Stawski et al., 2014), killifish (Furness, 2016) and birds (Ketterson et al., 2015). The theoretical studies that do consider seasonality are generally co-evolutionary with a gene-for-gene based infection interaction (Mostowy and Engelstädter, 2011; Nuismer et al., 2003; Poisot et al., 2012).
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2018, Hormones and BehaviorCitation Excerpt :Since circulating T levels do not reliably predict breeding readiness or timing in all species (Caro et al., 2006; Davies et al., 2015; Partecke et al., 2005; Schaper et al., 2012) studies incorporating more direct measures of HPG axis activity are necessary. Although several studies have noted links between endocrine breeding development (e.g. increasing T levels) and expression of migratory characteristics (Owen et al., 2014; Ramenofsky and Németh, 2014; Tonra et al., 2011), some of the behavioral and physiological effects linked to high T levels may be antagonistic to the expression of the migratory syndrome (Ketterson et al., 2015) and a successful migratory journey. For example, T-mediated territoriality while en route may be costly when a migrant is time constrained, which is especially likely during spring passage.
Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos (Junco hyemalis)
2016, General and Comparative EndocrinologyCitation Excerpt :The mechanisms generating divergent physiological trajectories in individuals exposed to the same conditions are unknown. Such comparisons between distinct groups known to differ in timing in response to identical cues provide a critical opportunity to characterize physiological diversification, and they also point towards useful methods that can be employed for more fine-scaled exploration of variation within populations (Ketterson et al., 2015). Specifically, we tested whether repeated GnRH injections (simulating episodic pulses of endogenous GnRH releases) exposes meaningful variation among resident versus migratory populations in downstream pituitary sensitivity.
Divergence along the gonadal steroidogenic pathway: Implications for hormone-mediated phenotypic evolution
2016, Hormones and BehaviorCitation Excerpt :Surprisingly, the direction of the population effect in StAR reversed signs from the wild to captivity, with VA captive males having more StAR mRNA than SD, despite SD still having higher expression of p450scc and CYP17. One interpretation is that the populations differ in some mechanism regulating reproductive timing (Ketterson et al., 2015), indicating that perhaps we did not compare them at equivalent stages of reproductive readiness. This potential confound is not supported, however, because the populations did not differ in gonad size, and the GnRH-induced T levels observed in captives were on par with those observed in the field for both populations (Jawor et al., 2006; Bergeon Burns, unpubl. data).