Elsevier Editorial System(tm) for Current Opinion in Behavioral Sciences Manuscript Draft Manuscript Number: COBEHA-D-15-00073R1 Title: Seasonal Timing and Population Divergence: When to Breed, When to Migrate Article Type: Integrated study of animal behavior (6) Corresponding Author: Professor Ellen Ketterson, Corresponding Author's Institution: Indiana University First Author: Ellen Ketterson Order of Authors: Ellen Ketterson; Adam Fudickar, Ph.D; Jonathan W Atwell, Ph.D; Timothy Greives, Ph.D Abstract: 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.
Detailed Response to Reviewers
Response to reviewers Editor's comments: Editors: This is an interesting and timely review that does an excellent job of summarizing the current state of the field. Both the reviewers and I enjoyed the manuscript greatly. Both reviewers give a number of suggestions to further improve the manuscript. I realize that you already were challenged for space, but I think try to squeeze in many of these ideas will make the manuscript better. My only really suggestion is that you might want to try and combine and/or extend some of those sections that are only one or two sentences long. I would also like to see the Introduction and Conclusion extended. Currently, each is only a single sentence long, which does not really achieve much! Thank you for the encouragement and the opportunity to improve the manuscript in part by expanding it. We have a longer Conclusion that refers to the Table and summarizes its main points. We also briefly describe what we see as the most important future directions. We have combined some other sections to make them longer and we removed some sub-headings so that the text flows more continuously. Reviewer #1: This review addresses the current understanding of how environmental conditions affect timing of breeding and migration with the intent of discerning how global climate change may influence each stage. Further consideration is given to the effects on populations and biodiversity in cases where the migratory phenotype is altered to such an extent that it is lost and the annual stages that once separated populations in time and place become sympatric resulting in changes in populations dynamics. The approach taken in the manuscript is to highlight new insights into the regulation and timing of both stages with information garnered from both captive and free-living studies. Variation in timing within and among populations This section points out that in cases where populations are exposed to the same environmental conditions they may diverge in when/where they reproduce. This is fascinating and to help explain the authors indicate probable differences in the perception, transduction and response to cues that result in fitness consequences. Although stated this can be more fully addressed by explaining that if populations are at different points in their annual cycle or different life history stages then the responses to a particular set of cues may be stimulatory to one but not effective to the other. I think these points may have been intended but are vague as presented and can be more fully developed that perception of the neuroendocrine system is dependent upon state of organism. A cue at one point may be significant but at another time not even perceived (mechanisms here are few and far between). Thus, if change is to occur the window of sensitivity to a particular environmental cue must change and the question becomes will this be through hybridization (if possible), mutation, epigenetic or other mechanisms. Any information on this front would be of great interest. We agree that if the environment is the same but animals are in different stages of their respective annual cycles they may differ in their response. So yes a cue that is meaningful to one population may not register with members of the other. We revised this section and I hope we captured the reviewer’s intention. Case in point is the sentence about allo- and heteropathy that it is possible that
hybridization could occur if the migrants are receptive to breeding residents but timing might not suggest that they are. The following paragraph may address this but comment needs to be made about different "states" and or stages that each is experiencing at these times. The piece quickly moves into the glucocorticoid realms and effects on breeding HPG axis related to stress. In most cases there is a documented delay in breeding but it is not clear how this will affect migration either its initiation or termination - intriguing problems. We agree that the question of how mechanisms associated with preparation to breed interact with mechanisms associated with preparation to migrate is largely unknown and we note that in the text and emphasize it in the revised conclusion Page 9 Explain what is meant by "metabolic stress" may be vague to some readers. We did this References some are incomplete We fixed these Seasonal timing here the point is made that for many but not all breeding is starting earlier and traveling shorter distances but the issue should be raised that for those breeding at higher latitudes and altitude or those pushing their geographic distributions the opposite may be true. Altitudinal migrants in some cases are traveling to great distances to avoid warming conditions and incidence of parasites including malaria, etc. In such cases later arrivals and longer distances traveled may be involved. In addition to the comment that starting to breed earlier is advantageous may not always be true particularly in more extreme environments where global change appears to have less of a warming effect and be more prevalent in terms of extreme events with serious consequences. We agree and we added a sentence to make this exact point Paragraph starting with Winker states that it is possible for migrant and resident populations to hybridize. If this is the case you need to add that if the breeding season of one extends to initiation of the other and if migrants stay put and achieve receptivity then this scenario can (and does) happen. One wonders how rare or common this is or becoming. This point is made more forcefully. We also do not know how rare or common this is but hope this paper will stimulate other people to seek answers. To avoid confusion under general heading of Timing of Reproduction. Clarify statements that if tendency for migratory populations declines and individuals remain on the wintering grounds this will increase the potential for hybridization. Conversely migratory populations remain on the breeding grounds and cease autumn movements then seasonal allopatry can become permanent and or sympatry with local breeders and may offer the chance to figure out what environmental conditions are contributing.
In conclusion the authors suggest that to understand issues of allochrony/heterochrony it is imperative to know how environmental cues influence the timing of migration and breeding timing. The authors wisely point out that the two are linked but how this works is unclear at present. To their credit they offer an impressive review of current and relevant literature focusing on regulation of breeding and migration. Many of the references refer to inhibitory effects on breeding (i.e. stress reactivity). This is important but the link with migration is weak. Problem being little is really understood about the regulation of onset of migration or flight itself, which is key to solving this conundrum as well as the transition from migration to breeding. Authors link the two in the final paragraph but we still are in the dark about the parallel pathways regulating the two processes. One paper that is informative - G Wang et al 2013 Current Zoology 59(3):349-359G - elucidating that the two pathways are distinct in terms photoreception and response. Agreed and again, the hope is that this contribution will cause more people to realize how rich this area is for research and what the implications are for loss or gain of biodiversity. We appreciate the reviewer directing us to the paper in current zoology and we have added it.
Reviewer #2: This review provides an overview of recent work on timing of reproduction and migration in the context of global change and gene flow. This article provides an important and novel perspective, highlighting recent research and also identifying important new directions for research. Overall this is an excellent review but I have some suggestions for potential improvement that the authors may want to consider. 1) In several sections the authors indicate that individuals that experience IDENTICAL conditions vary in timing of reproduction or migration. However, the idea that conditions are identical is likely not supported. For the timing of breeding, birds at a site may experience the same photoperiod but food, temperature, social cues etc are going to vary on a microgeographic scale. Thus the degree to which individual variation in timing results from individual differences vs microgeographic differences is not clear, and this should at least be acknowledged. We understand the reviewer’s point. In our own study system migrants and residents occur in the same flocks and are caught simultaneously in the same nets, so we were drawn to the word identical, but identity may not exist in anything ecological or behavioral. In any case, we have revised the text to say ‘nearly identical’ and we will proceed with caution. 2) One topic that is relevant but not covered here is individual variation in timing mechanisms. There are clearly individual differences in circadian rhythms, for example, and there is a huge literature on this. Species also vary in the amount of individual variation in timing mechanisms. For example, long distance migrants are typically less variable than short-distance migrants. A recent paper by Watts et al in JEZ-A shows that individual variation in photostimulation varies among species of birds. I understand the format for Current Opinions requires a short paper, but I think this concept should at least be briefly addressed.
We thank the reviewer for the opportunity to add words here and we now refer to the point s/he makes and to the paper by Watts et al. 3) The authors review recent research on stress reactivity and GnIH as a potential mechanism. The argument is that individual variation (IV) in stress reactivity could affect IV in timing of reproduction. However, isn't this just passing the buck? Where does the IV in stress reactivity come from? I think the argument here needs to be fleshed out in a little more detail, highlighting how geneenvironment interactions might produce IV in the stress response. Again we thank the reviewer for the chance to elaborate slightly. Conclusions: I found the reference to the Table a little too concise, and a few sentences here summarizing the main conclusions would be useful Agreed we have added to the Table caption and to the section entitled conclusions to describe the content of the Table Minor nit-picky points: Please include page numbers and line numbers. The term "behaviorist" has a long-established meaning with a particular emphasis on environmental determinism, and should probably not be used to describe animal behavior researchers in general. In a few places the authors use the phrase "perception-transduction-andresponse". This may be a term I'm not familiar with, but in sensory biology transduction must take place prior to sensation or perception. Similarly, perception is used in the review as synonymous with detection, which is not accurate. Stimuli are first transduced then there is sensation followed by higher level processing (perception). If the authors are referring to the detection and response to environmental cues that may not involve cognitive processing I'd recommend using terms other than perception. In the section on GR (citing reference 29) there are other studies on this from Liebl et al and Breuner, and seasonal changes in GR are not clear cut. In addition, there does not appear to be any correlation between GR mRNA and protein levels, so the story is more complicated than indicated.
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*Highlights (for review)
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
*Conflict of Interest
Conflict of interest statement Nothing declared.
*Manuscript
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Seasonal Timing and Population Divergence: When to Breed, When to Migrate
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Ketterson, Ellen D1, Fudickar, Adam M1, Atwell, Jonathan W1, and Greives, Timothy J2
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1
Indiana University, Department of Biology, 1001 E. Third Street, Bloomington, Indiana 47405
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USA 2
North Dakota State University, Department of Biological Sciences, 1340 Bolley Drive, Fargo, North Dakota 58102 USA
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Ellen D. Ketterson
1 812 855 6837
[email protected]
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Adam M. Fudickar
1 812 855-1096
[email protected]
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Jonathan W. Atwell
1 812 855-1096
[email protected]
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Timothy J. Greives
1 701 231-9461
[email protected]
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Corresponding author: Ellen D. Ketterson
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1
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Abstract
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Understanding how populations adapt to constantly changing environments requires
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approaches drawn from integrative and evolutionary biology as well as population ecology.
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Timing of reproduction and migration reflect seasonal pulses in resources, are driven by day
24
length, and are also responsive to environmental cues that change with climate. Researchers
25
focusing on birds have discovered accelerated breeding, reductions in migration, and extensive
26
variation in perception, transduction, and response to the environment. We consider situations
27
in which individuals experience the same environment but differ in the timing of the annual
28
cycle. Such scenarios provide exceptional opportunities to study mechanisms related to among-
29
population differences in timing (allochrony) and distribution (sympatry-allopatry-heteropatry),
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which have the potential either to enhance or reduce population divergence and biodiversity.
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Introduction
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The urgency of environmental change coupled with the availability of new technology is
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transforming our understanding of phenomena that have fascinated biologists for generations:
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changing seasons, seasonal shifts in behavior and morphology, and remarkable feats of
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migration. The last decade has seen an explosion of studies into seasonal timing that seek to
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identify how changing climates are altering the biology of seasonally breeding organisms [1].
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Emerging patterns in avian populations throughout the northern hemisphere include earlier
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breeding for many but not all species [1-4]. Migratory timing by birds has also been affected by
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warming [2,5-8]. Some species have shortened their migrations or ceased migrating altogether
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[6,9,10]. A related but distinct body of research has sought to elucidate the role of timing in
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phenotypic and genetic divergence among populations (see Table 1). Theoretical and empirical
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studies continue to challenge the view that speciation requires geographic isolation, and one
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focus has been to consider circumstances under which timing differences (allochrony) can give
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rise to reproductive isolation [11]. Studies of birds, plants, insects, fish, and bats have revealed
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among-population differences in timing that are interrupting gene flow, potentially leading to
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speciation [11-15].
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Seasonal timing and population divergence
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This contribution addresses how seasonality in the environment and timing of events of the
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annual cycle relate to population divergence by focusing on mechanisms of reproductive and
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migratory timing in birds. Working from the premise that selection acts on mechanisms that vary
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among individuals and populations and employing concepts and methods from three sub-fields,
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seasonality, evolutionary endocrinology, and geographic variation/population divergence, we
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briefly summarize what is new in the timing of reproduction and migratory biology as learned
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from intensive and prolonged study of individual bird species in the wild and in captivity.
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Variation in timing within and among populations
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It is almost a truism that members of a population experiencing the same environment will
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nevertheless differ among themselves in when they reproduce. Despite exposure to nearly
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identical day length, food supply, temperature, moisture etc., some individuals breed early and
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some breed later. While some of this variation can surely be attributed to age or condition,
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individuals are also known to be consistently early or late owing to their underlying biological
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timing.
66 67
The existence of this individual variation presents an outstanding opportunity to study
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mechanisms mediating timing and how they respond to selection. Early and late breeders can
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be compared for response to a particular day length, patterns of gene expression, sequence
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differences in candidate genes, systemic variation in perception-transduction-response to
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environmental cues [16], and fitness consequences of early and late reproduction. The same
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environmental cue might be stimulatory for some individuals and not for others at a different life-
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history stage and a critical question is why. In mice, individual variation in circadian rhythms
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was recently found to relate to distinct expression patterns of a key ‘clock’ gene, PER2, within
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the suprachiasmatic nucleus, the ‘master circadian oscillator’ [17]. It is likely that endogenous
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circadian rhythms influence seasonal photoperiodic timing decisions. Thus individual variation in
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timing mechanisms and responses to environmental cues may be influenced by photoperiodic
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history, history with other cues [17,18] and by genetic inheritance [19].
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These comparisons can also be made across populations of the same species that differ in
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timing of reproduction. High latitude or high altitude populations, for example, often breed later,
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providing natural comparisons. Interpretation of these comparisons is challenging, however,
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because so many factors may contribute to differences observed. Spring may come later at
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higher latitudes, but obviously so many other aspects of ecology differ as well.
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3
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Species consisting of sedentary and migratory populations that co-exist for portions of the year
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make it possible to study the mechanisms underlying timing of reproduction and migration.
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Cross-population comparisons of systemic physiology and gene expression in organisms
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experiencing the same environment become accessible. Such situations also make it possible
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to examine how within-population variation might alter gene flow and give rise to among-
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population variation and thus population divergence.
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Kevin Winker applied the term heteropatry to capture situations of ‘seasonal sympatry, seasonal
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allopatry,’ in which migrants and residents winter together in sympatry, but owing to the
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departure of migrants, breed in allopatry [1,20]. In such cases, residents typically initiate
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reproduction while migrants are still present, creating opportunities for hybridization that may or
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may not be realized. An important question is how such differences in timing in the same
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environment affect the likelihood of gene flow between migrants and residents. Do migrants
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mate with residents and give rise to ill-adapted young or do differences in timing prevent
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hybridization?
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Timing of reproduction and migration and biodiversity
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Comparisons of migrant and sedentary forms of the same species also raise the question of
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how migration-induced allopatry will respond to climate change and influence biodiversity.
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Future changes in animal movements may alter current patterns of overlap. If the tendency to
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migrate declines, such that currently allopatric breeding populations become sympatric, then
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opportunities for gene flow between migrant and sedentary forms may increase, leading to the
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merging of incipient species [21] and resulting in loss of nascent biodiversity. In other situations
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climate warming may lead to longer not shorter migrations, for example by migrants that
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currently breed at high altitudes. Finding favorable conditions for breeding that are currently
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achieved by flying uphill in spring may require a northward shift in latitude prior to breeding.
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Conversely, if formerly migratory forms become resident in portions of the breeding range from
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which they used to retreat, then populations that were sympatric in winter may now become
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allopatric year-round, reducing gene flow, reinforcing population divergence, and enhancing
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diversity. Combined study of mechanisms of timing, changes in animal movements, and niche
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modeling will contribute to predictions of the impact of environmental change on biodiversity.
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We turn now to selected advances related to determinants of when to breed and when to
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migrate as they bear on how seasonality in the environment and timing of the events of the
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annual cycle relate to population divergence.
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When to breed?
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Multiple reviews of selective consequences of within-population variation in timing have
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appeared recently [22-24]. In some cases, researchers have shown that breeding is taking
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place earlier in warm springs, that earlier breeding is leading to higher reproductive success,
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and that breeding dates are heritable. Researchers are also addressing how mechanisms of
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response to the environment relate to phenological change [16,25,26]. Nevertheless, much
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remains to be learned about how mechanisms related to timing of reproduction vary among
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individuals and populations.
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Onset of seasonal reproductive physiology and behavior has traditionally been studied as a
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response to seasonal changes in photoperiod (recently reviewed extensively [27]), but
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photoperiod and other measures of the external environment (e.g. food, temperature, etc.)
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cannot account for how individuals and populations experiencing the same immediate
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environment exhibit variation in how they respond. Early and late breeders within a population,
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and heteropatric populations that overwinter together but breed separately are prime subjects
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for addressing internal mechanisms by asking where variation lies at the level of the organism,
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particularly where variation lies along the reproductive hypothalamo-pituitary-gonadal (HPG)
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axis.
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One of many potential sources of within- and among-population variation is the interaction
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between stress reactivity and onset of reproduction. We have long known that individuals vary in
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how they prepare for and respond to ‘stressors’ [28,29], and that stress can dampen the activity
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of the HPG axis [30]. Thus, a prime candidate accounting for within- and among-population
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variation in timing is how stressors interact with the HPG during the critical window for timing
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decisions. Individuals with greater stress reactivity could be favored under certain environmental
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change scenarios, while individuals with lower stress reactivity could be favored under other
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scenarios [31]. Despite significant heritable variation in the avian stress response [32], all levels
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of the hypothalamo-pituitary-adrenal (HPA) axis can be altered during development, resulting in
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variations in adult phenotypes [33].
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Resident bird species prepare for reproduction by altering the functioning of the HPA which
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releases corticosterone (CORT), a glucocorticoid that is one of the primary contributors to the
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stress response [34]. In house sparrows (Passer domesticus) glucocorticoid receptor (GR)
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expression varies seasonally and a recent paper showed that GR binding in the brain is at its
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highest in the pre-egg laying period, suggesting a greater sensitivity to CORT during this critical
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timing window [35].
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Another way in which ‘stress reactivity’ may interact with the reproductive axis is via release and
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response to the neuropeptide, gonadotropin-inhibitory hormone (GnIH), which is expressed in
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the paraventricular nucleus (PVN) of the hypothalamus. GnIH is capable of down-regulating
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activity of the HPG axis via binding with receptors on the pituitary, and, potentially, via direct
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influence on GnRH neurons in the hypothalamus (reviewed in [23]). GnIH cells possess
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glucocorticoid receptors, and treatment with CORT increases GnIH mRNA expression *[36].
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Further, when norepinephrine, another signaling molecule that relates to stress, is injected into
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the PVN, quail increase GnIH mRNA transcription and GnIH release [37].
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In addition to potential influence at the levels of the hypothalamus and pituitary, glucocorticoids
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may directly influence the ability of the gonads to respond to the gonadotropins produced by the
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pituitary [38]. Testes of photosensitive European starlings (Sturnus vulgaris) stimulated with
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LH/FSH in vitro increase testosterone production, but this production is significantly diminished
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if CORT is also administered *[39]. However, when administered to fully mature testes, CORT
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fails to decrease testosterone secretion when compared to administration with LH/FSH alone.
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Food restriction or limiting resources would be predicted to delay the onset of reproduction.
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Administration of the drug 2-deoxyglucose (2-DG), a glucose analog inhibiting glycolysis, thus
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inducing a metabolic ‘stress,’ has been shown to up-regulate GnIH expression in the ovaries
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[39], suggesting a way in which resource availability might influence timing of reproduction.
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These studies indicate that individual/population variation in ‘stress reactivity’ may be a strong
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target for investigations of how timing differences may arise in the same environment. In
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populations that migrate, reproduction is delayed until migration has been accomplished. Thus
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another key question that is still almost entirely unanswered is how the mechanisms that time
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reproduction interact with those mediating migration. One recent paper provides new evidence
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that the pathways are independent and may be subject to distinct regulation [40].
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When to migrate?
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Returning to our objective of how seasonality in the environment and timing of the events of the
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annual cycle relate to population divergence, we turn to new developments in migratory timing
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in birds where rapid advances are taking place owing to new technology.
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Increasingly miniaturized geolocators, GPS loggers, satellite transmitters and other tracking
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devices deployed at breeding or wintering sites allow measurements of departure dates,
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migratory direction, duration and speed, and destination of migrations (for review of tracking
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technology see [41]). Recent advances in methods for interpreting intrinsic markers, such as
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stable isotopes and genetic markers, are adding to our knowledge of how breeding and
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wintering ranges of migratory species are connected [42-45], including the recent application of
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large numbers of genomic (SNP) markers [46]. Additionally, carefully coordinated and
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standardized citizen-generated databases (e.g. Cornell’s FeederWatch program) are providing
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invaluable information about the phenology and geography wild species in unprecedented ways
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[47,48].
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An important challenge is to relate these increasingly precise measurements of migratory
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geography and phenology in the wild to the mechanisms that regulate timing. Monitoring (or
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manipulating) hormones prior to migration is fostering correlative and experimental approaches
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for exploring the regulation of migration [49-51]. Further, studies of traditional measures of
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migratory readiness in caged migrants (fattening and nocturnal activity, referred to as migratory
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preparation) continue to be informative.
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Recent studies investigating the links between early activation of the HPG in preparation for
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reproduction and migration have identified a role for testosterone in both. Experimental
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elevation of testosterone in captive migratory gray catbirds (Dumetella carolinensis) induced
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earlier spring migration [52], and early elevation of testosterone prior to departure supported
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both migratory and breeding preparation in free-living American Redstarts [51]. However,
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testosterone alone is not sufficient for full expression of spring migration because castrated
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male white-crowned sparrows (Zonotrichia leucophrys gambelii) supplemented with
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testosterone fail to exhibit full migratory restlessness in spring [53].
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Increased food consumption and nocturnal activity characterize migrant birds during the season
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of migration and have been associated with seasonal elevation in baseline levels of the adrenal
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steroid corticosterone (CORT)[54-57]. However the pattern is not consistent across all species
7
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[58], and experimentally altering the HPA has had inconsistent effects on migratory preparations
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[59,60].
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Circulating levels of melatonin decrease in nocturnal migrants during the season of migration,
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suggesting that a reduction in melatonin may help to induce nocturnal activity [61,62]. However,
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experimental elevation of melatonin does not reduce nocturnal activity in migrating garden
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warblers (Sylvia borin) during stopover [63]. Individuals that had higher nighttime melatonin had
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greater diurnal activity and reduced body mass, indicating that reduced nighttime melatonin may
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play a role in energy conservation during migration [63].
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Mechanisms as constraint.
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Reproduction and migration have traditionally been viewed as distinct stages with little to no
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overlap in time or neuroendocrine control mechanisms [24,64]. However, newer findings reveal
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that preparation for spring migration and reproduction overlap in time and are tightly linked in
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mechanism [52,53,65]. An issue of controversy is the degree to which one life-history stage
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(migration) imposes a constraint on the ability of the other (reproduction) to respond
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independently to selection. For example, recent studies monitoring changes in timing of spring
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migration and reproduction have found that as one advances in response to changes in climate,
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so does the other [66,67], which is consistent with constraint. In White-crowned Sparrows
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exposed to green light during days that are long enough to stimulate gonadal growth if light is
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full spectrum exhibit migratory preparedness but not gonadal growth [40]. And a recent
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modeling paper [68], however, predicts that variation among species in length of the breeding
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season and timing of pulses of resources needed for breeding predict circumstances under
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which migratory and reproductive timing can evolve independently and that existing data are
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consistent with the model’s predictions. How reproductive and migratory timing respond to
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selection is fundamental to determining the role of timing (allochrony) in population divergence.
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Conclusion
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We conclude by referring the reader to Table 1, which contains a sampling of recent studies
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from 13 avian systems addressing integration of timing and population divergence. Collectively
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these studies serve as examples of what can be learned from examining the organismal and
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evolutionary mechanisms that facilitate population-level divergence in reproductive and
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migratory timing using a range of approaches including: measurements of gene expression,
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endocrine correlates of reproductive and migratory behavior, selection gradients, sequence
8
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variation in candidate genes, geographic variation in genetic structure and in timing, and
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comparisons of urban vs. wildland populations. As systems are added and more methods are
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applied to already studied systems, the role of timing mechanisms in promoting or reducing
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gene flow and population divergence will become clearer. Areas particularly deserving of more
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study include the impact of timing mechanisms on mate preferences, the role of early
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developmental environments on the expression of migratory and reproductive timing in adults,
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and the interaction of mechanisms that time migration and reproduction. Ultimately predicting
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short and longer-term responses to environmental change will require greater knowledge of
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where variation in timing mechanisms currently resides among individuals and across
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populations. In time we will learn what changes when a migrant becomes a resident and vice-
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versa, which will represent a major advance in our understanding of animal migrations.
265 266 267 268 269 270 271 272
Conflict of interest statement
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• of special interest
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•• of outstanding interest
Nothing declared. References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:
275 276 277
Acknowledgements We thank the National Science Foundation [IOS- 1257474(E.D.K.) and IOS-1257527 (T.J.G)],
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our many talented collaborators who contributed ideas and constructive criticism, two
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anonymous reviewers who provided excellent suggestions for improvement, and editors
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Hoffman and Rubenstein.
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Table 1 Recent studies of avian systems addressing integration of timing and population divergence by employing measurements of gene expression, endocrine correlates of reproductive and migratory behavior, selection gradients, sequence variation in candidate genes, geographic variation in genetic structure and in timing, and variation in urban vs. wildland populations.
Study System Great tits Parus major
Great & Blue Tits Blue tits Cyanistes caeruleus European blackbirds Turdus merula
Blackcaps Sylvia atricapilla
Barn swallows Hirundo rustica
Dark-eyed junco Junco hyemalis
White-crowned sparrow Zonotrichia leucophrys Pied Flycatcher Ficedula hypoleuca Florida scrubjay, Aphelocoma coerulescens Rufous-collared sparrows, Zonotrichia capensis Stonechats Saxicola spp. Seabirds
290 291 292 293
Approaches / References Gene expression differences among populations that differ in latitude, following photoperiod treatment [69] Candidate genes in relation to timing of breeding within a population, including selection analysis* [70] Longitudinal studies of selection on endocrine correlates of timing of breeding within a population [71] Divergence in timing of breeding among urban vs. wildland populations in relation to artificial light [72] Integration of candidate gene and quantitative genetic approaches [73] Candidate genes for timing of breeding within- and among-pops. across latitude [74,75] Endocrine correlates of timing among closely related populations inhabiting different localized climates Longitudinal studies of selection on timing of breeding within and among populations [76] Divergence in timing among urban vs. wildland populations in relation to artificial lighting [72] Common garden studies of timing of breeding and migration (Zugunruhe), including endocrine correlates in urban vs. wildland populations [8,77-79] Loss of migration and neutral genetic divergence among multiple urban vs. wildand populations [80] Divergence in reproductive timing in urban vs. wildland populations relation to artificial light [72] Candidate genes for timing and others traits among multiple urban vs. wildland population pairs* [81] Divergence among urban vs. wildland populations in timing in relation to artificial lighting [72] Candidate genes for migratory distances among (& within) populations [82] Artificial selection (disruptive), leading to loss of migratory propensity [83] Ecological mechanisms (eco-morphology) in relation to divergence in migratory populations across latitude [84] Divergence in timing of (migratory) arrival and breeding phenology among sympatric cohorts, including analyses of neutral genetic divergence [85,86] Analysis of neutral genetic divergence among variably migratory populations across latitude / longitude [14] Candidate (Clock) genes in relation to timing of breeding, migration, life-history and molt, within and among populations, including longitudinal studies of selection [87,88] Loss of migratory behavior (shifts northwards) in relation to climatic warming [89] Endocrine correlates of divergence in timing of breeding in urban vs. wildland populations also inhabiting distinct localized climates, including common garden studies [90,91] Loss of migration in an urban vs. wildand populations, including common garden approach (Zugunruhe) Candidate genes for migratory distance within- & among-populations across latitude & urban vs. wildland* [92] Common garden for timing of breeding across latitude, incl. endocrine correlates in seasonal sympatry [93] Gene expression in relation to divergent in timing & migratory strategy across latitude & urban vs. wildland** Divergence in reproductive timing, migratory strategies, and life-history among closely related populations & subspecies, including endocrine correlates of divergence [94,95]*** Experimental studies of seasonal gene expression in relation to altered photoperiod and hormonal conditions [96] Longitudinal studies of selection on candidate genes & neutral genetic divergence within and among populations across latitude / longitude [97] Candidate genes (Clock, ADCYAP1) in relation to timing of migration among individuals during migration [98] * Endocrine correlates in relation to divergence in timing among urban vs. wildland populations, including evaluation of ecological mechanisms [99] Divergence in timing (asynchrony) and neutral genetic divergence among two adjacent equatorial populations inhabiting different localized climates [100], including studies of endocrine correlates
Common garden for timing of breeding and migration (Zugunruhe) among populations across latitude [101] Cross-breeding to evaluate fitness consequences of reproductive timing in ‘hybrid’ pairs [101,102] Neutral genetic divergence and timing of breeding differences within & among island populations in sympatry [15] Ecological mechanisms (habitat specialization, non-breeding segregation) underlying allochrony in sympatry [103] Ecological mechanisms (energetics) in relation to divergent migratory strategy & allochrony under sympatry [104]
* These studies chiefly report negative results (i.e. lack of associations) **Current research in progress by A. Fudickar et al. ***Also see ongoing research by M. Ramenofsky and Z. Németh
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