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Temperature-Dependent Sex Determination in Vertebrates Temperature-Dependent Sex Determination in Vertebrates Temperature-Dependent Temperature-Dependent VALENZUELA AND LANCE Sex Determination in Vertebrates EDITED BY Nicole Valenzuela and Valentine A. Lance * Smithsonian Books Smithsonian * Smithsonian Books Temperature-Dependent Sex Determination in Vertebrates Temperature-Dependent Sex Determination in Vertebrates Nicole Valenzuela and Valentine Lance Smithsonian Books Washington © 2004 by Smithsonian Institution All rights reserved Copy editor: Bonnie J. Harmon Production editor: Robert A. Poarch Designer: Brian Barth Library of Congress Cataloging-in-Publication Data Temperature-dependent sex determination in vertebrates / edited by Nicole Valenzuela and Valentine A. Lance. p. cm. Includes bibliographical references and index. ISBN 1-58834-203-4 1. Sex (Biology). 2. Vertebrates. I. Valenzuela, Nicole. II. Lance, Valentine A. QP278.5.T45 2004 571.8’16—dc22 2004042882 British Library Cataloguing-in-Publication Data available Manufactured in the United States of America 10 09 08 07 06 05 04 1 23 4 5 ⅜∞ The paper used in this publication meets the minimum requirements of the American National Standard for Information Sciences—Permanence of Paper for Printed Library Materials ANSI Z39.48-1984. For permission to reproduce illustrations appearing in this book, please correspond directly with the owners of the works. Smithsonian Books does not retain reproduction rights for these illustrations individually. Contents Introduction 1 Chapter 1 Perspective on Sex Determination: Past and Future 5 . Part 1 Prevalence of Temperature-Dependent Sex Determination in Vertebrates Chapter 2 Temperature-Dependent Sex Determination in Fishes 11 . Chapter 3 Turtle Sex-Determining Modes and TSD Patterns, and Some TSD Pattern Correlates 21 . , . , . Chapter 4 Prevalence of TSD in Crocodilians 33 . Chapter 5 Temperature-Dependent Sex Determination in Lizards 42 . Chapter 6 Temperature-Dependent Sex Determination in Tuataras 53 . , , . , . , . Chapter 7 Thermal Sex Reversals in Amphibians 59 , -, , , vi Contents Part 2 Thermal Effects, Ecology, and Interactions Chapter 8 General Effects of Temperature on Animal Biology 71 . Chapter 9 Thermal Models of TSD under Laboratory and Field Conditions 79 , , , Chapter 10 Phenotypic Effects of Incubation Temperature in Reptiles 90 . Chapter 11 The Temperature-Dependent Sex Determination Drama: Same Cast, Different Stars 99 . . Chapter 12 Yolk Steroid Hormones and Their Possible Roles in TSD Species 111 . Part 3 Evolutionary Considerations Chapter 13 Phylogenetics: Which Was First, TSD or GSD? 121 . . Chapter 14 Evolution and Maintenance of Temperature-Dependent Sex Determination 131 Chapter 15 Implications of Temperature-Dependent Sex Determination for Population Dynamics 148 , , , , - -, . Conclusions: Missing Links and Future Directions 157 Literature Cited 161 Contributors 187 Index 191 NICOLE VALENZUELA Introduction This Book how is it maintained, and will it prevail? (4) What do we still need to learn about it? Almost four decades after the discovery of temperature- In Chapter 1, J. J. Bull offers an enlightening perspective dependent sex determination (TSD) in vertebrates credited in the field of temperature-dependent sex determination to Charnier (1966), we find ourselves faced with a vast through an historical account of his own experience in the amount of information related to this mechanism that has area. Chapters 2–7 in Part 1 encompass a series of reviews been gathered by researchers from a variety of disciplines. with additional new data on the incidence of TSD in fish, The most comprehensive review on TSD was included in turtles, crocodilians, lizards, and tuataras, and on the inci- the well-cited book by J. J. Bull (1983), Evolution of Sex De- dence of thermal sex reversals in amphibians, including some termining Mechanisms. The field of TSD has come a long discussion about the ecological or evolutionary significance way since then, and twenty years after Bull’s publication we of particular cases. Chapters 8–12 in Part 2 provide the felt there was a need for a new volume dedicated exclusively reader with some basics about the general effects of tem- to this subject. perature on animal biology, and then describe what is known This book represents such an attempt and is intended as about how temperature affects development and sex ratios a comprehensive work that compiles, analyzes, and integrates under lab and field conditions for TSD species, about ther- existing information about this sex-determining mecha- mal effects on phenotypic traits other than sex, about the nism. This volume encompasses a series of reviews of what molecular network underlying genotypic and temperature- is known about the ecological, physiological, molecular, dependent sex determination, and about the influence of and evolutionary aspects of TSD. We tried to bring to- yolk steroids in sex-determination/differentiation. Chapters gether, for the first time, the diversity of issues related to 13–15 in Part 3 present a new phylogenetic analysis explor- this sex-determining mechanism and synthesize the vast lit- ing the ancestry of the sex-determining mechanisms in ver- erature from multiple disciplines. The book is organized in tebrates, and review the postulated hypotheses explaining four thematic sections: Prevalence of Temperature-dependent TSD’s past and present evolution, as well as the interactions Sex Determination in Vertebrates; Thermal Effects, Ecology, among TSD, sex-ratio production, and population dynam- and Interactions; Evolutionary Considerations; and Conclu- ics, including an analysis relevant to some conservation sions: Missing Links and Future Directions. These sections issues. correspond to basic questions about TSD: (1) Who pos- In the second part of this introduction, I provide a brief sesses TSD? (2) How does it work? (3) How did it appear, background section about vertebrate sex-determining mech- 1 2 Introduction anisms and define the most commonly used terminology 2003). Temperature can also alter sex differentiation and related to temperature-dependent sex determination. Sev- induce sex reversal in species possessing sex chromosomes eral chapters provide more detailed descriptions of some of (Dournon et al. 1990; Baroiller et al. 1995; Solari 1994; see these terms and phenomena, but this introduction should also Chardard et al., Chapter 7), resulting in biased second- suffice as a general guideline. ary sex ratios. Lastly, some vertebrate species do not display We hope that researchers, students, and other inter- sex chromosomes; no consistent genetic differences exist ested readers find this volume a useful reference resource, between the sexes, so that sex cannot be predicted by zygotic and that it fosters new investigations in this exciting field. As genotype; and sex determination occurs after fertilization, editors, we are indebted to each and every author who so by incubation temperature (Bull 1983; Solari 1994; Valen- enthusiastically contributed to this book and to the many zuela et al. 2003). In this last system (i.e., temperature- reviewers who evaluated manuscripts, often on very short dependent sex determination or TSD), primary sex ratios notice. are not defined at conception: they are realized after fertil- ization, according to the incubation temperature, and can General Background often be biased (Valenzuela et al. 2003). Vertebrate Sex-Determining Systems Temperature-Dependent Sex Determination Not all animal species determine sex in the same fashion. In Under TSD, the sex of individuals is indifferent until deter- many vertebrates, sex is determined by major sex factors mined permanently after conception, by incubation tem- contained in sex chromosomes (Bull 1983), which can differ perature (Bull 1983). Among vertebrates, TSD is unknown morphologically from each other (heteromorphic) or not in snakes, birds, mammals, and amphibians, is infrequent in (homomorphic) (Bull 1983; Solari 1994). In some species fishes (although new reports are increasing), but is very (XX/XY), males are heterogametic (XY), whereas in other common in reptiles—it occurs in all studied crocodilians species (ZZ/ZW), females are heterogametic (ZW) (Bull and tuataras, is prevalent in turtles, and more infrequent in 1983). Heteromorphic sex chromosomes are present in am- lizards (reviewed in Chapters 2–7). Although there is a wide phibians, reptiles, fishes, birds, and mammals (Bull 1983; agreement on the definitions of TSD and GSD as described, Solari 1994 and references therein). Many amphibian and fish only recently has an explicit set of criteria been proposed to species possess homomorphic sex chromosomes (e.g., Winge identify the presence of TSD unambiguously (Valenzuela et and Ditlevsen 1948; Yamamoto 1969; Kallman 1984; reviewed al. 2003). in Solari 1994). Genotypic sex determination (GSD) systems Three modes of temperature-dependent sex determi- different from the classic XX/XY and ZZ/ZW include ver- nation are recognized, categorized according to the sex ra- tebrates in which more than one X or Y chromosome is tios produced as a function of incubation temperature (Fig- normally present per individual, others where three or more ure I.1A). In TSD II (also called female-male-female or FMF sex chromosome types segregate in the population, and a pattern), low and high temperatures produce females, few species where a group of minor sex-determining genes while intermediate temperatures produce males. In TSD Ia
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