REVIEWS
“An interesting, thorough, and timely summary of decades of work on juncos. It will be of interest to not only ornithologists, but also behavioral ecologists, comparative physiologists, and evolutionary biologists.”
— Zachary Cheviron, University of Montana
“An excellent, very readable, comprehensive, and diverse set of papers. It is clear the authors have made a great effort to integrate two perspectives, with several chapters dealing with this explicitly. The combination of the very strong existing reputation of the Ketterson lab, including substantial, significant contributions to the integration of organismal and evolutionary biology, with the broad appeal of the junco, a common, widely distributed species familiar to many, will make for a popular tome.”
— Tony D. Williams, Simon Fraser University, author of "Physiological Adaptations for Breeding in Birds"
“I truly enjoyed reading Snowbird! The book is aimed at scientific readers, but it is written very elegantly, providing an easy and pleasant read. Even though it focuses on one species complex, it is amazingly broad in its approach, ranging from historic aspects of junco research to biogeography, taxonomy, endocrinology, behavior, evolution, speciation, sexual selection, and other topics. The authors did an excellent job in explaining the concepts that guided their research, thus appealing to both specialists and a broader audience of readers. The last chapter of the book is devoted entirely to outlining future research areas, again both in specific and broader areas of biology, which will be very useful for everyone aiming at continuing in the spirit of integrative research on major organismal questions. Snowbird will be an important addition to the scientific literature.”
— Michaela Hau, Max Planck Institute for Ornithology
“A must have for anyone with a serious interest in juncos.”
— Ian Paulsen, Birdbooker Report
“Snowbird is about juncos, but it is about so much more than a small genus of birds. The contributors to this volume have done a wonderful job of illustrating how a research focus on just one taxonomic group can greatly benefit multiple fields of biology. . . . A well-planned, integrative volume. . . . The final chapter is presciently titled, ‘Standing on the Shoulders.’ . . . Snowbird represents an impressive set of shoulders on which to stand and guide us as we learn about our natural world.”
— Jerry Husak, University of St. Thomas, Journal of Field Ornithology
“Longitudinal studies of organisms in the wild are the gold standard for understanding the complexity and dynamics of the evolutionary process. . . . Snowbird is focused on a songbird that has become a workhorse for integrative long-term research: the dark-eyed junco. . . . However, this book is much more than an exploration of a particular bird: it is an authoritative example of how to do integrative biology thoroughly, and thoroughly well.”
— Rebecca J. Safran, University of Colorado, Boulder, Evolution
“In Snowbird, editors Ketterson and Atwell have pulled together a book that captures the best of the species-account tradition while delving into issues of mechanisms that might better reflect the model system approach. . . . Unusual and valuable. . . . It will be interesting to see if this book will stimulate additional treatments at the species level that try to integrate ecology/evolutionary thinking with work on physiological mechanisms. Both communities could benefit from such thinking.”
— Gregory F. Ball, University of Maryland, Animal Behaviour
“Within North America, the Junco, or snowbird, is frequently spotted in numerous locations. Ketterson and Atwell dive into a thorough discussion of the biological aspects of this bird species. Topics within the work include species evolution, sex hormone experimentation, adaptation to novel habitats, breeding and social interactions, song development, and possibilities and outlooks for future research. The Junco is presented as a bird with a quick rate of evolution; currently, there are fifteen recognized subspecies. In a few locations, reproductive isolation occurs between some Junco taxonomies. This work, which is intended for students and ‘science professionals,’ is readily accessible. The chapters that discuss hormonal research and song development will be especially valuable for future researchers. Also, this book will pique the interest of general readers, who may have spied a few types of Junco in their own backyard. By reading this title, scientists and birders will gain new respect for this small songbird. Recommended.”
— M. Gochfeld, Rutgers Robert Wood Johnson Medical School, Choice
TABLE OF CONTENTS
Introduction -Ellen D. Ketterson and Jonathan W. Atwell
DOI: 10.7208/chicago/9780226330808.003.0001
[integrative organismal biology, speciation, population divergence]
This chapter describes what is covered in the book as a whole, laying out its structure and intellectual themes. (pages 1 - 8)
This chapter is available at:
University of Chicago Press
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The junco: a common bird and a classic subject for descriptive and experimental studies in evolutionary and integrative biology -Ellen D. Ketterson and Jonathan W. Atwell
DOI: 10.7208/chicago/9780226330808.003.0002
[Alden Miller, American Ornithologists Union (AOU), annual cycle, Ernst Mayr, Jonathan Dwight, migration, photoperiodism, speciation, William Rowan, Zugunruhe]
This chapter describes how an ordinary 'little gray bird' became extraordinary because of its appeal to bird watchers and its fascination for scientists interested in how species form and how they time their migrations and other events of the annual cycle. The chapter introduces researchers who studied the junco in earlier times and shows how their contributions paved the way for the junco's current role as a model for study in evolutionary and organismal biology. (pages 11 - 34)
This chapter is available at:
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Axes of biogeographic variation in the avian genus Junco: habitat, morphology, migration, and seasonal timing, with implications for diversification under heteropatry -Jonathan W. Atwell, Dawn O'Neal, and Ellen D. Ketterson
DOI: 10.7208/chicago/9780226330808.003.0003
[biogeography, ecology, habitat, heteropatry, life history, migration, morphology, natural history, phenology, phenotype]
Evaluating organismal and evolutionary mechanisms that underlie diversification requires detailed biogeographic information about phenotypes and environments, and is particularly informative, though challenging, in widely distributed, highly mobile animals that occupy a broad range of habitats, as does the genus Junco. Important goals such as elucidating evolutionary histories and examining local adaptation are also made more challenging when considering migratory populations that are allopatric when breeding but sympatric at other times of year. This pattern of distribution ('heteropatry,' Winker 2010a) raises important questions about the interplay between local adaptation and gene flow in facilitating and maintaining diversification in variably migratory lineages such as Junco. Chapter 3 provides an overview of both well-studied and largely underexplored 'axes of biogeographic variation'—habitat, morphology, migration, and seasonal timing—that characterize different junco populations, noting glaring gaps in basic natural history information for many groups. It also discusses the potential roles of variation in seasonality and migration in maintaining or reinforcing diversification among junco populations in the context of heteropatry, and raises future research avenues for improving the resolution of phenotypic and geographic characterizations of variation, including a major role for emerging technologies. (pages 35 - 66)
This chapter is available at:
University of Chicago Press
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Phenotypic engineering: a long-term study using hormones to study life history trade-offs and sexual conflict -Nicole M. Gerlach and Ellen D. Ketterson
DOI: 10.7208/chicago/9780226330808.003.0004
[testosterone, selection, life histories, trade-offs, hormones, experimental manipulations, sexual conflict, sex differences]
In natural systems, time and resources are finite and must be allocated between competing life history demands. Allocation is frequently mediated by the endocrine system, and study of the relationships among hormones, behavior, and fitness has helped to reveal how conflicts inherent in life histories are resolved. From 1987-2007, we employed experimental manipulations of testosterone to study trade-offs in a natural population of juncos. Phenotypes of male juncos with experimentally elevated testosterone differed from controls. Alterations in male physiology and behavior resulted in reduced fecundity with social mates and decreased survival, but greater overall reproductive success due to more extra-pair offspring. Female physiological and behavioral responses to increased testosterone were somewhat similar, but the fitness consequences were highly detrimental. These results suggest that increased testosterone is favored in males but not females, suggesting sexual conflict, and perhaps accounting for maintenance of testosterone at levels below the male optimum. However, the evolutionary dynamics underlying this system are almost certainly more complicated. The degree to which testosterone-mediated traits are beneficial to males may be frequency dependent or may vary among years. These additional considerations may shape both the proximate regulation and the evolution of hormone-mediated life history traits. (pages 71 - 99)
This chapter is available at:
University of Chicago Press
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Hormonal pleiotropy and the evolution of correlated traits -Joel W. McGlothlin and Ellen D. Ketterson
DOI: 10.7208/chicago/9780226330808.003.0005
[hormones, testosterone, adaptation, constraint, correlational selection, phenotypic integration]
One of the fundamental properties of hormones is that they underlie the expression of suites of correlated traits. To the extent that this hormonal mediation has a genetic basis, hormones may act to either accelerate or slow adaptive evolution. Selection on one trait within a hormone-mediated suite may lead to evolutionary changes in other traits mediated by the same hormone, which may be either beneficial or detrimental. As such, mediation by a common hormone can be seen as the analog of genetic pleiotropy. In this chapter, we discuss how variation in endocrine pathways should affect the evolutionary process, and in turn, how natural selection should be expected to shape such pathways. We argue that in order to achieve a fuller understanding of the roles of hormones in evolution, we must study naturally occurring variation—which is the raw material for natural selection—in addition to performing experiments in phenotypic engineering. Studies of natural variation in hormones and hormone-mediated traits, such as the work in juncos described in chapters 6 and 7, may provide important insights about the extent to which hormonal pleiotropy reflects the results of adaptive evolution versus a constraint on future evolution. (pages 100 - 119)
This chapter is available at:
University of Chicago Press
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Individual variation & selection on hormone-mediated phenotypes in male and female dark-eyed juncos -Kristal Cain, Jodie M. Jawor, and Joel W. McGlothlin
DOI: 10.7208/chicago/9780226330808.003.0006
[Gonadotropin-releasing hormone (GnRH), testosterone, aggression, parental care, individual variation, GnRH challenge, Dark-eyed junco]
Much of our knowledge of hormones and life histories in animals derives from experimental studies. Complementing experiments with studies of natural (co)variation in hormones and hormone-mediated traits can lead to a richer understanding of the role of hormones in the evolutionary process. Here, we review our work on natural variation in testosterone production and its relationships to hormone-mediated traits and fitness in male and female juncos. To assess variation in testosterone production, we used injections of gonadotropin-releasing hormone (GnRH), which induce repeatable measures of an individual's ability to produce testosterone. Testosterone production stimulated by GnRH was associated with hormone-mediated behaviors such as aggression and parental care, as well as morphology and several components of fitness. Some of these relationships mirrored the results of experimental manipulations and some did not; possible reasons for the differences are discussed. This research provides an intriguing glimpse of how selection may shape variation in hormones and hormone-mediated phenotypes in natural populations. (pages 120 - 147)
This chapter is available at:
University of Chicago Press
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Diving deeper into mechanism: individual and sex differences in testosterone production, sensitivity, and genomic responses -Kimberly A. Rosvall, Christine M. Bergeon Burns, and Mark P. Peterson
DOI: 10.7208/chicago/9780226330808.003.0007
[Androgen receptor, gene expression, genomic tools, HPG axis, individual variation, integration/independence, LH receptor, sex differences, steroid sensitivity]
If we are to understand how hormone-mediated traits evolve, we need to examine the mechanisms underlying individual and sex differences in hormones and their effect on physiology, behavior, and ultimately fitness. This chapter begins to unravel this mechanistic black box, focusing on individual and sex variation in production of testosterone (T), sensitivity to T, and the downstream effects of T on organismal biological processes, employing the dark-eyed junco as a model. Correlational and experimental studies at each of these levels of analysis reveal a remarkable degree of independence among the constituent parts of the endocrine system. Further, although the sexes show striking similarities in the abundance of transcript for sex steroid binding and processing molecules at neural targets, the downstream genomic effects of hormones differ between males and females. Thus, while hormonal pleiotropy produces suites of correlated traits, individual variation in circulating T, sensitivity to T, and T-mediated gene expression exists along many different axes within the endocrine system, providing a multitude of different mechanisms on which selection could act. Likewise, the sexes appear to have found partial solutions to sexual conflict over T at each of these parts of the endocrine system, particularly with respect to the downstream genomic effects of T. (pages 148 - 176)
This chapter is available at:
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More than meets the eye: lineage diversity and evolutionary history of dark-eyed and yellow-eyed juncos -Borja Milá, Pau Aleixandre, Sofía Alvarez-Nordström, and John McCormack
DOI: 10.7208/chicago/9780226330808.003.0008
[phylogeography, speciation, systematics, allopatric divergence, diversification]
Molecular genetic tools are helping us to reconstruct the evolutionary history of juncos and thus to understand the factors, mechanisms and timing of their diversification. A new phylogeny based on sequence from the cytochrome c oxidase I gene and including all main junco groups confirms the recent diversification of dark-eyed juncos within the last 10,000 years, and reveals that lineages in isolated areas such as Baja California, Guadalupe Island and the highlands of Guatemala have been isolated for hundreds of thousands of years, yet they have differentiated relatively little in plumage color. We conclude that some phenotypic traits, such as eye color and several plumage color traits are labile and not phylogenetically informative, whereas others such as bill color or song characters are more consistent with lineage history. Long-term geographic isolation seems to be the main factor driving the divergence of Guatemala, Baird's and Guadalupe juncos, whereas a role for selection must be invoked to explain the rapid divergence of continental dark-eyed junco taxa from yellow-eyed juncos. Based on currently available data and practical considerations, we propose that six species-level taxa be recognized within the genus. (pages 179 - 198)
This chapter is available at:
University of Chicago Press
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The potential role of parapatric and allo-parapatric divergence in junco speciation -Trevor D. Price and Daniel Hooper
DOI: 10.7208/chicago/9780226330808.003.0009
[allo-parapatric, speciation, chromosomal inversions, parapatric speciation, Pleistocene climate]
Speciation may occur as a result of complete divergence in allopatry, or proceed in the face of ongoing migration between populations (parapatric speciation). Gene exchange may also occur intermittently during divergence if populations contract and expand their ranges, occasionally coming in contact (allo-parapatric speciation). We consider these modes of divergence in the establishment of color differences between geographically separated taxa of North American juncos. First, we describe a modern-day junco example of the early stages of differentiation despite gene flow, the result of a resident population becoming established from an over-wintering one in UC San Diego. That population appears to continue to receive immigrants as result of over-wintering birds remaining to breed. Second, across the North American junco complex, climate reconstructions imply multiple range shifts through the Pleistocene, but an important refuge in Alaska. We suggest a novel hypothesis that integrates these observations to explain the low genetic diversity in neutral markers but strong color differences among taxa: individuals from populations of seasonal migrants occasionally interbreed with residents to the south, resulting in directional gene flow from north to south, and an effective population size estimated from neutral markers that is close to that of the northern most populations. Chromosomal inversions, which are known to be present in the junco, may aid differentiation at certain genomic regions. (pages 199 - 222)
This chapter is available at:
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Shifts in hormonal, morphological, and behavioral traits in a novel environment: comparing recently diverged Junco populations -Jonathan W. Atwell, Danielle J. Whittaker, Trevor D. Price, and Ellen D. Ketterson
DOI: 10.7208/chicago/9780226330808.003.0010
[adaptation, boldness, climate change, corticosterone, divergence, microevolution, phenoology, rapid evolution, testosterone, urbanization]
In a rapidly changing world, understanding how organisms and populations respond to new or changing environments is of importance for addressing challenges related to conservation of biodiversity, ecosystem function, and human health. Contemporary colonization events provide a rare opportunity to study developmental and evolutionary responses to novel environments in 'real time.' In this chapter, we provide a comprehensive review of nearly two decades of research examining a unique Junco colonization event in S. California, in which a typically montane-breeding subspecies (J.hyemalis thurberi) recently (c. 1983) established a small population in an urban and coastal environment. First, we discuss the unique natural history of this study system. Second, we summarize observed phenotypic changes in behavior, morphology, and physiology that have been documented to date, including evidence for both [developmental] plasticity and rapid [genetic] evolution, inferred from field and common garden studies. Third, we discuss the relevance of these studies in the wider context of efforts to link integrative and evolutionary biology by studying hormones and hormone-mediated traits. We conclude by exploring the promise of ongoing and future work in this system, including a scope for adding replicate population comparisons from other Junco colonizations of urban habitats and offshore islands. (pages 225 - 262)
This chapter is available at:
University of Chicago Press
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A physiological view of population divergence: comparing hormone production and response mechanisms -Christine M. Bergeon Burns and Kimberly A. Rosvall
DOI: 10.7208/chicago/9780226330808.003.0011
[divergence, individual variation, phenotypic integration, testosterone, HPG axis, hormone receptor]
Coordinated expression of multiple traits by a hormone can promote an integrated phenotype. Such phenotypic integration can be adaptive if the traits mediated by hormones are most adaptive when co-expressed, but integration may have important consequences for the tempo or ease of evolutionary change. For example, tight integration may hinder the expression of new combinations of traits that may be favored under changing selection pressures. The degree of integration is likely to depend on lability of many links in the complex mechanistic pathway from environmental stimulus to phenotypic response in the face of selection. In this chapter, we explore divergence in testosterone (T)-mediated traits from a mechanistic perspective. We compare two phenotypically distinct dark-eyed junco subspecies, reviewing both upstream variation in T production mechanisms, and downstream variation in sensitivity to T at target tissues. Our analyses suggest that endocrine response mechanisms may be more prone to divergence than circulating hormone levels. An important pattern emerging from these studies is that existing sources of individual variation in endocrine mechanisms (upon which selection may currently act) are not always reflected in differences between populations (that may reflect past selection), posing questions about the evolutionary mechanisms driving diversification. (pages 263 - 280)
This chapter is available at:
University of Chicago Press
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Mate choice in dark-eyed juncos using visual, acoustic, and chemical cues -Danielle J. Whittaker and Nicole M. Gerlach
DOI: 10.7208/chicago/9780226330808.003.0012
[mate choice, sexual selection, sexual signals, chemical signals, olfaction, plumage ornaments, extra-pair mating]
In this chapter, we explore the traits used for mate recognition and assessment in the dark-eyed junco. Much research has focused on visual cues, in particular the plumage trait known as tail white, and less on acoustic cues like long-range and short-range song. We consider a third dimension of communication that is often completely overlooked when considering mate choice in birds: olfaction. We review what is known so far about the production, detection, and use of scents in courtship. Finally, we consider the various contexts of mate choice in a socially monogamous system, the limits of female mate choice, how mate choice can be assessed by experimental and observational means, and how it may affect sexual selection and population differentiation. (pages 281 - 309)
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Dark-eyed junco song: linking ontogeny and function with a potential role in reproductive isolation -Gonçalo C. Cardoso and Dustin G. Reichard
DOI: 10.7208/chicago/9780226330808.003.0013
[song evolution, short-range song, low-amplitude song, song functions, geographic variation, cultural learning, novel songs, acoustic adaptation, sexual selection, repertoire size]
The elaborate songs produced by many songbirds during the breeding season play an integral role in mate attraction and courtship. Depending on how song is learned and develops, it may diverge rapidly across space and promote reproductive isolation. Here we review the function, ontogeny and geographic divergence of dark-eyed junco song, to evaluate its potential as an isolating mechanism. Dark-eyed juncos share long-range songs (LRS) minimally with other males within populations, populations harbor high diversity of LRS, acoustic properties of LRS vary little across subspecies, and males respond aggressively to songs from distant populations. We suggest that a high input of novel song types during song development has a homogenizing effect on song properties across populations, which hinders reproductive isolation. In contrast, junco short-range songs (SRS) are much more complex than LRS, and may be less constrained by acoustic transmission properties because they are close-proximity signals. Thus, the acoustic properties of SRS may be more evolutionarily labile in response to changes in female preference or other selective pressures, and could play a greater role promoting divergence among populations. We also discuss functionally puzzling aspects of dark-eyed junco song development, and emphasize the importance of addressing entire vocal repertoires when investigating sexual selection and reproductive isolation. (pages 310 - 337)
This chapter is available at:
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Standing on the shoulders: agendas for future research addressing evolutionary and integrative biology in a rapidly evolving songbird -Ellen D. Ketterson and Jonathan W. Atwell
DOI: 10.7208/chicago/9780226330808.003.0014
[Arginine vasopressin, Bergmann's Rule, correlational selection, ecology, Gloger's Rule, heteropatry, microevolution, niche modelling, urban ecology]
This chapter builds on 'priorities for future research' as laid out in the species' accounts of the dark-eyed and yellow-eyed junco in Birds of North America in 1999 and 2002. It also relates directions for future research as described by the book's authors during discussions following the junco summit held at Indiana University in 2012 (see Preface) and in their chapters. It concludes with a small number of specific recommendations for how to advance the integration of organismal and evolutionary biology. (pages 338 - 356)
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