In the Light of Evolution
Volume X: Comparative Phylogeography
JOHN C. AVISE and FRANCISCO J. AYALA, Editors
NATIONAL ACADEMY OF SCIENCES
THE NATIONAL ACADEMIES PRESS
Washington, DC
www.nap.edu
THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001
This volume is based on the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution X: Comparative Phylogeography,” held January 8–9, 2016, at the Arnold and Mabel Beckman Center of the National Academies of Sciences, Engineering, and Medicine in Irvine, California. It is the tenth (and final) in a series of annual colloquia under the umbrella title “In the Light of Evolution.”
The articles appearing in these pages were contributed by speakers at the colloquium and have been anonymously reviewed. Any opinions, findings, conclusions, or recommendations expressed in this volume are those of the authors and do not necessarily reflect the view of the National Academy of Sciences.
Cataloging-in-Publication Data
In the light of evolution / John C. Avise and Francisco J. Ayala, editors.
p. cm.
Vol. I based on a colloquium of the National Academy of Sciences, held
December 1–2, 2006, in Irvine, California.
Includes bibliographical references.
ISBN-13: 978-0-309-44422-4
ISBN-10: 0-309-44422-5
1. Evolution (Biology)—Congresses. I. Avise, John C, 1948–. II . Ayala, Francisco José, 1934–III . National Academy of Sciences (U.S.)
QH359.I55 2007
576.8—dc22
2007032455
Digital Object Identifier: 10.17226/23542
Additional copies of this publication are available for sale from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu.
Cover image: Space (geography) and time (genealogy) are the two axes that constitute the framework of comparative phylogeography. Albert Einstein demonstrated that space and time are connected in astrophysics; phylogeographers are showing that space and time often display relatable patterns in biology also. Drawing by John C. Avise.
Suggested citation: Avise, John C., and Francisco J. Ayala, Eds. 2017. In the Light of Evolution, Volume X: Comparative Phylogeography. Washington, DC: The National Academies Press. doi: 10.17226/23542.
Copyright 2017 by the National Academy of Sciences. All rights reserved.
Printed in the United States of America
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Arthur M. Sackler, M.D. 1913–1987
Born in Brooklyn, New York, Arthur M. Sackler was educated in the arts, sciences, and humanities at New York University. These interests remained the focus of his life, as he became widely known as a scientist, art collector, and philanthropist, endowing institutions of learning and culture throughout the world.
He felt that his fundamental role was as a doctor, a vocation he decided upon at the age of four. After completing his internship and service as house physician at Lincoln Hospital in New York City, he became a resident in psychiatry at Creedmoor State Hospital. There, in the 1940s, he started research that resulted in more than 150 papers in neuroendocrinology, psychiatry, and experimental medicine. He considered his scientific research in the metabolic basis of schizophrenia his most significant contribution to science and served as editor of the Journal of Clinical and Experimental Psychobiology from 1950 to 1962. In 1960 he started publication of Medical Tribune, a weekly medical newspaper that reached over one million readers in 20 countries. He established the Laboratories for Therapeutic Research in 1938, a facility in New York for basic research that he directed until 1983.
As a generous benefactor to the causes of medicine and basic science, Arthur Sackler built and contributed to a wide range of scientific institutions: the Sackler School of Medicine established in 1972 at Tel Aviv University, Tel Aviv, Israel; the Sackler Institute of Graduate Biomedical Science at New York University, founded in 1980; the Arthur M. Sackler Science Center dedicated in 1985 at Clark University, Worcester, Massachusetts; and the Sackler School of Graduate Biomedical Sciences, established in 1980, and the Arthur M. Sackler Center for Health Communications, established in 1986, both at Tufts University, Boston, Massachusetts.
His pre-eminence in the art world is already legendary. According to his wife Jillian, one of his favorite relaxations was to visit museums and art galleries and pick out great pieces others had overlooked. His interest in art is reflected in his philanthropy; he endowed galleries at the Metropolitan Museum of Art and Princeton University, a museum at Harvard University, and the Arthur M. Sackler Gallery of Asian Art in
Washington, DC. True to his oft-stated determination to create bridges between peoples, he offered to build a teaching museum in China, which Jillian made possible after his death, and in 1993 opened the Arthur M. Sackler Museum of Art and Archaeology at Peking University in Beijing.
In a world that often sees science and art as two separate cultures, Arthur Sackler saw them as inextricably related. In a speech given at the State University of New York at Stony Brook, Some reflections on the arts, sciences and humanities, a year before his death, he observed: ‘‘Communication is, for me, the primum movens of all culture. In the arts . . . I find the emotional component most moving. In science, it is the intellectual content. Both are deeply interlinked in the humanities.’’ The Arthur M. Sackler Colloquia at the National Academy of Sciences pay tribute to this faith in communication as the prime mover of knowledge and culture.
Contents
Preface to the In the Light of Evolution Series
Preface to In the Light of Evolution, Volume X: Comparative Phylogeography
PART I COMPARATIVE PHYLOGEOGRAPHY IN A SPATIAL SENSE
1 Comparative Phylogeography of the Ocean Planet
Brian W. Bowen, Michelle R. Gaither, Joseph D. Di Battista, Matthew Iacchei, Kimberly R. Andrews, W. Stewart Grant, Robert J. Toonen, and John C. Briggs
3 Inferring Responses to Climate Dynamics from Historical Demography in Neotropical Forest Lizards
Ivan Prates, Alexander T. Xue, Jason L. Brown, Diego F. Alvarado-Serrano, Miguel T. Rodrigues, Michael J. Hickerson, and Ana C. Carnaval
Kerry L. Shaw and Rosemary G. Gillespie
PART II COMPARATIVE PHYLOGEOGRAPHY IN A GENOMIC SENSE
5 Effects of the Population Pedigree on Genetic Signatures of Historical Demographic Events
John Wakeley, Léandra King, and Peter R. Wilton
6 The Probability of Monophyly of a Sample of Gene Lineages on a Species Tree
Rohan S. Mehta, David Bryant, and Noah A. Rosenberg
7 Phylogeographic Model Selection Leads to Insight into the Evolutionary History of Four-Eyed Frogs
Maria Tereza C. Thomé and Bryan C. Carstens
8 Toward a Paradigm Shift in Comparative Phylogeography Driven by Trait-Based Hypotheses
Anna Papadopoulou and L. Lacey Knowles
9 Reticulation, Divergence, and the Phylogeography–Phylogenetics Continuum
Scott V. Edwards, Sally Potter, C. Jonathan Schmitt, Jason G. Bragg, and Craig Moritz
PART III COMPARATIVE PHYLOGEOGRAPHY IN A TAXONOMIC SENSE
10 Global Biogeography of Microbial Nitrogen-Cycling Traits in Soil
Michaeline B. Nelson, Adam C. Martiny, and Jennifer B. H. Martiny
Kelly R. Zamudio, Rayna C. Bell, and Nicholas A. Mason
Anne D. Yoder, C. Ryan Campbell, Marina B. Blanco, Mario Dos Reis, Jörg U. Ganzhorn, Steven M. Goodman, Kelsie E. Hunnicutt, Peter A. Larsen, Peter M. Kappeler, Rodin M. Rasoloarison, José M. Ralison, David L. Swofford, and David W. Weisrock
Peter D. Heintzman, Duane Froese, John W. Ives, André E. R. Soares, Grant D. Zazula, Brandon Letts, Thomas D. Andrews, Jonathan C. Driver, Elizabeth Hall, P. Gregory Hare, Christopher N. Jass, Glen MacKay, John R. Southon, Mathias Stiller, Robin Woywitka, Marc A. Suchard, and Beth Shapiro
14 Evolutionary Lessons from California Plant Phylogeography
Victoria L. Sork, Paul F. Gugger, Jin-Ming Chen, and Silke Werth
15 Human Phylogeography and Diversity
PART IV COMPARATIVE PHYLOGEOGRAPHY IN A CONCEPTUAL SENSE
Preface to the In the Light of Evolution Series
Biodiversity—the genetic variety of life—is an exuberant product of the evolutionary past, a vast human-supportive resource (aesthetic, intellectual, and material) of the present, and a rich legacy to cherish and preserve for the future. Two urgent challenges, and opportunities, for 21st-century science are to gain deeper insights into the evolutionary processes that foster biotic diversity, and to translate that understanding into workable solutions for the regional and global crises that biodiversity currently faces. A grasp of evolutionary principles and processes is important in other societal arenas as well, such as education, medicine, sociology, and other applied fields including agriculture, pharmacology, and biotechnology. The ramifications of evolutionary thought also extend into learned realms traditionally reserved for philosophy and religion.
In 1973, Theodosius Dobzhansky penned a short commentary entitled “Nothing in biology makes sense except in the light of evolution.” Most scientists agree that evolution provides the unifying framework for interpreting biological phenomena that otherwise can often seem unrelated and perhaps unintelligible. Given the central position of evolutionary thought in biology, it is sadly ironic that evolutionary perspectives outside the sciences have often been neglected, misunderstood, or purposefully misrepresented.
The central goal of the In the Light of Evolution (ILE) series is to promote the evolutionary sciences through state-of-the-art colloquia—in the series of Arthur M. Sackler colloquia sponsored by the National Academy of Sciences—and their published proceedings. Each installment explores
evolutionary perspectives on a particular biological topic that is scientifically intriguing but also has special relevance to contemporary societal issues or challenges. Individually and collectively, the ILE series aims to interpret phenomena in various areas of biology through the lens of evolution, address some of the most intellectually engaging as well as pragmatically important societal issues of our times, and foster a greater appreciation of evolutionary biology as a consolidating foundation for the life sciences.
The organizers and founding editors of this effort (Avise and Ayala) are the academic grandson and son, respectively, of Theodosius Dobzhansky, to whose fond memory this ILE series is dedicated. May Dobzhansky’s words and insights continue to inspire rational scientific inquiry into nature’s marvelous operations.
John C. Avise and Francisco J. Ayala
Department of Ecology and Evolutionary Biology, University of California, Irvine (January 2007)
Preface to In the Light of Evolution, Volume X: Comparative Phylogeography
Phylogeography is the study of the spatial arrangement of genealogical lineages, especially within and among conspecific populations and closely related species (Avise, 2000). Ever since its inception in the late 1970s (Avise et al., 1979a,b) and mid-1980s (Avise et al., 1987), the field has sought to extend phylogenetic reasoning to the intraspecific level, and thereby build empirical and conceptual bridges between the formerly separate disciplines of microevolutionary population genetics and macroevolutionary phylogenetics. In the early years, phylogeographers relied on data from restriction-site surveys of mitochondrial (mt) DNA to draw inferences about population structure and historical demography, but stunning improvements in molecular techniques (Emerson et al., 2010; Rocha et al., 2013) and extensions of coalescent theory and other analytical methods (Knowles, 2009b) later broadened the field’s scope dramatically (Hickerson et al., 2010). Phylogeographic perspectives have transformed aspects of population biology, biogeography, systematics, ecology, genetics, and biodiversity conservation. One aim of this colloquium was to bring together leading scientists to address the current state of phylogeography as the discipline enters its fourth decade. The broader goal was to update a wide audience on recent developments in phylogeographic research and their relevance to past accomplishments and future research directions.
Many of the advancements in phylogeography have entailed comparative appraisals of one sort or another (Bermingham and Moritz, 1998). Chapters in Part I of this volume emphasize the word “comparative” in a spatial sense, where the phylogeographic assessments entail various
species (sometimes generally codistributed) that may be representative of particular kinds of environmental settings, such as oceanic versus continental realms. Part II deals with comparative phylogeography in a genomic sense. Nonrecombining cytoplasmic genomes have been the standard workhorses of genealogical analyses, but in principle the primary library of evolutionary histories is ensconced in nuclear genomes that are increasingly accessible to scrutiny. Part III focuses on comparative phylogeography in a taxonomic sense, emphasizing how phylogeographic findings have impacted ecological and evolutionary thought in a wide diversity of organismal groups. Part IV focuses on comparative phylogeography in a conceptual sense by addressing the place of phylogeography in relation to various allied disciplines in the biodiversity sciences. Several chapters in this book inevitably overlap in their sectional assignments because, for example, disparate taxa tend to inhabit different environments, and because the researchers assembled here had a diversity of phylogeographic objectives, data types, and analytical approaches.
This is the tenth and final edition of the “In the Light of Evolution” series. Previous colloquia in this series dealt with the following topics: I, Adaptation and Complex Design (Avise and Ayala, 2007); II, Biodiversity and Extinction (Avise et al., 2008); III, Two Centuries of Darwin (Avise and Ayala, 2009); IV, The Human Condition (Avise and Ayala, 2010); V, Cooperation and Conflict (Strassmann et al., 2011); VI, Brain and Behavior (Striedter et al., 2012); VII, The Human Mental Machinery (Cela-Conde et al., 2013); VIII, Darwinian Thinking in the Social Sciences (Skyrms et al., 2014); and IX, Clonal Reproduction: Alternatives to Sex (Tibayrenc et al., 2015). We hope that this “In the Light of Evolution” series has indeed enlightened a broad audience about the many manifestations and marvelous biological products of our planet’s diverse evolutionary processes.