Evolution of vulnerability implications for sex differences in health and development

Evolution of Vulnerability Evolution of Vulnerability Implications for Sex Differences in Health and Development David C Geary AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier To Yin Academic Press is an imprint of Elsevier 125 London Wall, London, EC2Y 5AS, UK 525 B Street, Suite 1800, San Diego, CA 92101–4495, USA 225 Wyman Street, Waltham, MA 02451, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK © 2015 Elsevier Inc All rights reserved No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein) Notices Knowledge and best practice in this field are constantly changing As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress For information on all Academic Press publications visit our website at http://store.elsevier.com/ Printed in the United States of America ISBN: 978-0-12-801562-9 Preface The seeds of this book – that sexual selection can be used to more fully understand sex differences in vulnerability to stressors – were planted during the writing of the first edition of Male, Female (Geary, 1998), and fleshed out a bit in the second edition (Geary, 2010) As was the case with Male, Female and the other books I have written, I thought about the concept and how to approach this book for several years; of course, I also managed to get a few others things done in the meantime Although my primary interests are with human vulnerabilities, I decided that it was important to conduct an extensive review of condition-dependent traits in nonhuman species These reflect an individual’s level of exposure to and ability to tolerate various types of stressors, such as poor nutrition or parasites I spent nearly a year on this review, during which I prepared extensive tables of these traits and the stressors that affect them across a very diverse array of species These nonhuman studies helped me to better understand condition-dependent traits and the associated reviews and tables are, I believe, useful in and of themselves, whether or not the reader is interested in human vulnerability The primary goal however was to address the inevitable objections to my thesis that exposure to stressors will affect boys and girls and men and women differently and in ways that are only understandable when framed in an evolutionary perspective Whatever objections may arise to my thesis, I believe the extensive reviews of condition-dependent traits in nonhuman species and the simple evolutionary concept that ties them together provides a solid foundation for the study of human vulnerabilities As the reader will see, I used this foundation to make predictions about when in development, and for which sex, exposure to stressors will be most harmful to the expression of specific physical, behavioral, and brain and cognitive traits As I did for nonhuman species, I used these predictions to organize reviews of empirical research on how poor nutrition, disease, and exposure to social stressors (e.g., childhood maltreatment) and toxins affected the development and expression of these traits Conducting these reviews was at times an exercise in frustration, as many of the studies that included the traits of interest did not report sex differences, and many of the studies that did report these differences assessed traits that I suspected won’t be particularly vulnerable for either sex Nevertheless, I found enough extant research to show how exposure to various types of stressors can differentially affect the physical, social, and brain and cognitive health and development of ix x  Preface boys and girls and men and women I hope that the associated reviews will provide a useful foundation for the future study of human vulnerabilities During the writing of this book, I contacted various experts to ask questions about one matter or another and asked some of them to read and critique one or all of the chapters I acknowledge and thank them: Dan Berch, Kingsley Browne, Napoleon Chagnon, Martin Daly, David Epstein, Carl Gerhardt, Jeffrey Gilger, Alex Moore, and Amanda Rose I want to especially acknowledge and thank my former students, Drew Bailey and Benjamin Winegard, who critiqued the entire book, and Eldin Jašarević, who helped me flesh out these ideas in many thoughtful discussions and during our collaborative work on the topic I also thank Sarah Becktell for double checking all of the references in the text and tables, and Mary Hoard and Lara Nugent for expertly managing the day-to-day operations of the lab while I was distracted by this project Most important, my deepest thanks go to my wife Yin Xia, the love of my life Without her continual support and kindness, I may have never completed this book David C Geary January 16, 2015 Chapter Vulnerability Chapter Outline The Value Added by an Evolutionary Perspective Nonhuman Vulnerabilities Human Vulnerabilities Conclusion The question of whether one sex or the other is more vulnerable to stressors is an intriguing and important one Historically, the question has focused on the issue of male vulnerability (e.g., Greulich, 1951; Stini, 1969; Stinson, 1985) Even Darwin (1871) noted the excess of premature male mortality in many species, including the higher mortality of boys than girls during infancy It is indeed the case that boys are more likely to die in infancy than girls, even with the dramatic declines in overall mortality over the past two centuries (Martin, 1949; Read, Troendle, & Klebanoff, 1997), and surviving boys are overrepresented among children with mild to serious medical or physical conditions (Jacobziner, Rich, Bleiberg, & Merchant, 1963) It is also the case that young men die at higher rates than young women – often as a direct result of maleon-male aggression (Wilson & Daly, 1985) or due to status seeking “showing off” (e.g., reckless driving; Evans, 2006) – and that men have a shorter life span than women (Allman, Rosin, Kumar, & Hasenstaub, 1998) These are certainly important vulnerabilities and can be placed in the context of the evolution of life histories (e.g., environmental influences on the timing of reproductive competition), some of which are discussed in Nesse and Williams’s (1996) introduction to evolutionary medicine (see also Belsky, Steinberg, & Draper, 1991; Ellis, 2004; Figueredo et al., 2006) However, they are not my focus Rather, I am interested in the more nuanced questions of why some traits – specific physical features, behaviors, or cognitive competencies – are more easily disrupted by exposure to stressors than others, and why these trait-specific vulnerabilities can differ between the sexes and across species For instance, why does poor nutrition during adolescence affect the height and physical fitness of boys more than girls (Prista, Maia, Damasceno, & Beunen, 2003), but the early stage of Alzheimer’s disease affects the language competencies of women more than men (Henderson, Watt, & Galen Evolution of Vulnerability http://dx.doi.org/10.1016/B978-0-12-801562-9.00001-6 © 2015 Elsevier Inc All rights reserved 2  Evolution of Vulnerability Buckwalter, 1996)? In broader perspective, why does prenatal exposure to toxins compromise the spatial-navigation abilities of male deer mice (Peromyscus maniculatus), but leave unaffected the spatial abilities of same-­species females or males of their cousin species, the California mouse (Peromyscus californicus; Jašarević et al., 2011; Williams et al., 2013) Vulnerability from a life history perspective, in contrast, is focused on how exposure to stressors influences the timing (not disruption) of reproductive traits, such as age of menarche, or modifies how sexual relationships are formed and maintained (Del Giudice, 2009; Ellis & Del Giudice, 2014) Again, these are important issues, but beyond the scope of what I wish to accomplish in this book My goal is to outline and provide evidence for a simple conceptual model – traits that have been elaborated through sexual or social selection are ­especially vulnerable to disruption by exposure to environmental and social stressors – that allows us to understand the vulnerabilities of adolescent boys, women with Alzheimer’s disease, and male deer mice, among many others, and places all of them in a unifying evolutionary context The model enables the identification of sex- and species-specific traits whose development and expression are vulnerable to disruption by disease, poor nutrition, social stressors, and exposure to man-made toxins (e.g., environmental toxins and chemotherapy) The concept that pulls cross-species vulnerabilities together is found with Darwin’s (1871) sexual selection – competition for mates and mate choices – and West-Eberhard’s (1983) social selection – competition for reproductively relevant resources (e.g., high-quality food) other than mates The key is that these social dynamics result in the evolutionary exaggeration of traits that facilitate competition or that make one attractive to mates These traits are either signaled directly (e.g., through physical size) or indirectly (e.g., through plumage coloration that is correlated with diet quality) and can be physical, behavioral, or involve brain and cognition, as will be illustrated in subsequent chapters Whatever the trait, they are effective signals because they convey information about the individual’s level of exposure to stressors and the ability to cope with them Identifying these traits and the conditions that can disrupt their expression is complicated, however, because a trait that signals competitive ability, for instance, in one sex or species may or may not signal competitive ability in the other sex or in other, even closely related species (Andersson, 1994) For either sex or any species, the identification of vulnerable traits requires an understanding of the evolutionary history of the species, in particular the traits that facilitate competition for mates and other resources and that influence mate choices I provide the background needed to understand competition and choice and the sensitivity of the associated traits to environmental and social stressors in Chapter 2 and illustrate the ubiquity and diversity of these traits in Chapters 3 and I then apply these same principles to humans and detail the traits that I ­predict will be more vulnerable to stressors in boys and men, and the traits that Vulnerability  Chapter | 1  3 I predict will be more vulnerable in girls and women The existing literature on human sex differences does not allow for an evaluation of all of these predictions, but I provide proof of concept illustrations of sex differences in physical and behavioral vulnerabilities in Chapter 6 and in brain and cognitive vulnerabilities in Chapter 7 Implications for understanding and studying the nuances of human vulnerabilities are discussed in Chapter 8 I outline some of the key points of subsequent chapters in the second section below In the first, I provide a few thoughts on why an evolutionary perspective on human vulnerabilities is important THE VALUE ADDED BY AN EVOLUTIONARY PERSPECTIVE There are many things in the world that can be harmful to people, including premature birth, pre- and postnatal exposure to toxins, poor nutrition, infestation with parasites, poverty, and childhood maltreatment, among others Indeed, these risks are well recognized and in many cases extensively studied (e.g., Hotez et al., 2008; Kim & Cicchetti, 2003), but they have not been framed in terms of sex differences in risk The key to fully understanding the consequences of exposure to these potential hazards is to understand the traits that are most likely to be affected by them, and when in development these traits are most likely to be disrupted Without this knowledge, we may assess traits that are not strongly affected by risk exposure, miss those that are affected, or assess the right traits but at the wrong time or in the wrong sex The result is an underestimation of the consequences of exposure or even a determination that exposure has no deleterious consequences at all Moreover, without a conceptual framework for understanding vulnerability, it is also possible that sex differences for one especially vulnerable trait are overgeneralized to all traits, as seemed to have happened historically with boys’ early mortality risks and a general belief in “male vulnerability.” As I illustrate in Chapter 2, there is good reason to believe that infection with any number of parasites – viruses, bacteria, worms – will compromise health and development Indeed, the relation between parasite infestation and many features of children’s and adults’ physical, behavioral, and cognitive competencies have been assessed for more than a century (Dickson, Awasthi, Williamson, Demellweek, & Garner, 2000; Watkins & Pollitt, 1997), including recent studies in Zaire (Boivin et al., 1993), the Philippines (Ezeamama et al., 2005), Tanzania (Grigorenko et al., 2006), Brazil (Parraga et al., 1996), and Indonesia (Sakti et al., 1999), among others (Adams, Stephenson, Latham, & Kinoti, 1994) Whether one uses an evolutionary framework or not, it is clear to most people that many physical traits and their development differ for boys and girls Thus, most of the studies of physical growth or fitness reported results for both sexes This allowed me to better situate these findings in the context of sexual selection and thereby test specific predictions about when in ­development illness will similarly affect boys and 4  Evolution of Vulnerability girls (childhood) and when (puberty) and which traits will be differentially affected in boys (e.g., height) and girls (e.g., pelvic width), as we will cover in Chapter 6 At the same time, most of the studies that assessed cognitive or behavioral outcomes collapsed boys and girls or men and women into a single group, included sex as a “nuisance” variable (and did not report any effects of sex), or assessed outcomes that will be less sensitive to parasite exposure than many of the traits I review in Chapter 5 A similar pattern is evident in studies of the long-term consequences of premature birth (e.g., Caravale, Tozzi, Albino, & Vicari, 2005; Crnic, Ragozin, Greenberg, Robinson, & Basham, 1983), the social consequences of childhood maltreatment (Kim & Cicchetti, 2003), and the potential cognitive deficits resulting from chemotherapy (Vardy, Rourke, & Tannock, 2007), to mention just a few As I argue in Chapter 5, there are good a priori reasons to believe that boys and men and girls and women, as well as children and adults, will respond to these stressors in different ways Using studies that did report sex differences, I illustrate these sex- and age-specific vulnerabilities in Chapters 6 and The overall result of ignoring sex has been an underappreciation of how exposure to stressors can affect some traits but not others and an underestimation of the deleterious effects of these stressors If we want a more complete and nuanced understanding of how exposure to stressors can disrupt human health and development, most of these studies will need to be redone I outline the traits that are most likely to show sex-specific disruptions to stressors in Chapter 5, and in Chapter 8 I elaborate on implications for better assessing these vulnerabilities in future studies NONHUMAN VULNERABILITIES To appreciate and fully understand my evolutionary framing of human vulnerabilities, an introduction to how sexual and social selection work over evolutionary time and how they are expressed in nonhuman species is necessary As noted, I provide these fundamentals in Chapter 2, focusing on the relation between competition and choice and sex differences in physical (e.g., body size), behavioral (e.g., courtship displays), and brain and cognitive (e.g., as related to bird song) traits In comparison to naturally selected traits – those important for survival (Darwin, 1859) – the development and expression of the traits that have been exaggerated by competition and mate choice are especially sensitive to environmental and social conditions Stated differently, the full expression of these traits requires not only the right combination of genes, but also good environmental (e.g., low parasite levels) and social (e.g., parental provisioning) conditions during development and in adulthood Individuals with this mix of genes and experiences are more likely to fully develop these traits than are other individuals and as a result have competitive advantages and are preferred as mates 396   Author Index Snow, D.A., 24 Snowdon, C.T., 129–139, 133t Snyder, R.J., 23, 24, 140 Söffker, M., 80 Soha, J.A., 31 Soini, H.A., 208 Soler, A.J., 126t Soler, M., 173 Solomon, N.G., 23 Sommer, A., 184, 186t, 203 Soneira, S., 232–246, 233t Song, Y.M., 198 Sood, S., 268t, 276 Soorya, L.V., 211t Sorace, A., 37, 38, 150 Sorci, G., 25–26, 30, 44t, 52t, 56t, 72–73 Sorokin, E.S., 133t Sosis, R., 266 Sotres-Bayon, F., 265–266 Southall, B., 133t Southwick, S.M., 253t, 267, 268t Souza Lopes, A.C., 6, 185–198, 186t Sowell, E.R., 170–171, 180–181 Sparks, A., 210–219, 211t, 220, 286 Sparrow, D., 253t Specht, K., 142–143, 170, 227–228, 266–267 Spelke, E.S., 166–167 Spencer, K.A., 5–6, 31, 35, 38, 56t, 61t, 77, 78, 79–80, 266 Spiers, H.J., 170 Spies, T.D., 185–198, 186t Spinetta, M., 37 Spiro, A., 253t Spisak, B.R., 167 Spritzer, M.D., 23 Spry, N., 253t, 264, 265 Sripada, C.S., 268t, 276 Sripada, R.K., 268t, 276 Sripiroj, P., 199t, 207–208 Stahl, W., 199t, 207–208 Stallings, V.A., 185–198, 186t Stanton, S.J., 170, 266–267, 288 Steere, P.L., 142 Stein, J.L., 170–171 Stein, K., 250–251 Stein, M.B., 268t Stein, Z., 253t Steinberg, F., 283 Steinberg, L., Steiner, B., 253t Steiner, V.G., 286–287 Steinhauer, S.R., 211t, 227, 253t, 262 Stephen, I.D., 117–118, 172–173, 206–208 Stephenson, L.S., 3–4, 186t, 203, 287 Stepick, C.D., 186t, 199t, 203 Sternberg, R.J., 3–4 Stevens, J.R., 37 Stevens, M., 44t, 71–73, 210–219, 211t, 220 Stevenson, I.R., 28–29, 124–125, 126t Stickel, L.F., 292–293 Stieglitz, J., 225–226 Stini, W.A., 1, 182, 186t, 228, 232 Stinson, S., 1, 7, 182, 185, 228, 232 Stirrat, M., 186t Stockley, P., 12, 27 Stodola, D.E., 267, 268t Stoehr, A.M., 96–97 Stoltzfus, R.J., 172–173, 185, 186t Stone, V., 166–167, 232 Strassmann, B.I., 172, 174 Stringer, C., 160 Strobeck, C., 124–125, 126t Strobel, D.A., 142 Strough, J.-N., 179 Strube, M.J., 167 Stubbs, V.C., 283 Stucky, B.D., 173–174 Stulp, G., 186t Sudakov, M., 172, 174–175, 177 Suhonen, J., 96–97, 98t, 101t, 113t Sukumar, R., 130t Sullivan, M.S., 30 Sullivan, S., 233t, 245–246 Sumner, K., 37 Sumner, P., 117–118 Sundaram, R., 174–175 Sundermann, C.A., 44t, 290–291 Sung, J., 198 Surai, P.F., 44t, 66–67 Surridge, A.K., 117–118 Susser, E.S., 211t, 226–227 Susser, M., 253t Sutalo, S., 130t Sutherland, R.J., 263–264 Sutherland, W.J., 19–20, 69 Svensson, P.A., 35, 42, 66–67, 72 Svrakic, D., 288 Swan, S.H., 7–8, 210–220, 211t, 219f, 286 Swartz, R.J., 252 Sweeting, H., 222, 279–280 Swenson, L.P., 179, 288 Swerdloff, R.S., 253t Syhre, M., 209 Számadó, S., 30 Székely, T., 101t Author Index    397 Sznycer, D., 186t, 206 Szuran, T.F., 143–150, 144t Szykman, M., 29 T Takahashi, H., 15 Takahira, S., 168 Takeuchi, Y., 133t, 141–142, 168 Tal, I.R., Tamarin, R.H., 24 Tanese, R., 33 Tanner, J.M., 160–161, 184, 203, 286, 287 Tanner, S., 7, 186t, 199t Tannock, I.F., 4, 233t Tapajóz Pereira de Sampaio, F., 232–246, 233t Taper, M., 101t, 110–111, 150–151 Tarvin, K.A., 35, 41, 44t, 70, 94, 151 Tarwotjo, I., 184, 186t, 203 Taskinen, J., 96–97, 101t, 113t Taylor, A., 260–261, 286–287 Taylor, H.G., 165, 175, 221, 233t, 247 Taylor, J.S., 262–263 Taylor, S.E., 165, 175, 221, 233t, 247 Tchanturia, K., 8, 232–246, 233t, 280 Tchen, N., 233t te Nijenhuis, J., 225 Te Velde, E.R., 173 Teicher, M.H., 171 Teichroeb, J.A., 133t Teixeira, C.M., 23 Templeton, A., 32 ter Maat, A., 79–80 Terracciano, A., 225 Thal, L.J., 233t Thatcher, G.W., 268t, 276 Theriault, R.L., 233t, 251 Thiessen, D.D., 125–139, 133t Thomas, C.L., 186t Thomas, J.R., 164–165, 204–205, 286 Thomas, L., 173–174, 175–176, 229 Thompson, M.E., 29 Thompson, P.J., 170 Thompson, P.M., 277–278 Thoms, H., 199t Thomson, I.R., 113t Thonhauser, K.E., 130t Thor, D.H., 133t Thornhill, R., 5–6, 41–42, 44t, 52t, 72–73, 101t, 111, 173, 208 Thoß, M., 130t Thune, I., 173 Thurstone, L.L., 289 Tian, D., 133t, 140, 144t Tibbetts, E.A., 6, 101t, 109–110, 151–152 Tielsch, J.M., 185, 186t Timonen, T., 233t Tingen, C.M., 283 Tobias, J.A., 26, 151–152 Todd, K.L., 142–143 Todisco, P., 233t, 245–246 Toft, G., 82t, 84t Toga, A.W., 170, 227–228, 266–267 Toïgo, C., 6, 126t, 184 Toledo, M.I., 179 Tolin, D.F., 225 Tolle, A.E., 113t Tomkins, J.L., 32–33, 113t Tomoeda, C.K., 233t Tong, S., 253t, 262 Tooby, J., 186t, 206 Torchia, M.G., 268t Torio, A.J., 82t, 92t, 290–291 Török, J., 52t, 56t, 77 Torrealba, I., 184, 185–198, 186t Torres, R.H., 117–122 Torrey, W.C., 278–279 Tostain, O., 5–6, 56t, 76–77 Tottenham, N., 266–267 Touhara, K., 209 Towler, S., 168–169, 180–181, 281 Towson, S.M.J., 167 Tozzi, C., Tranel, D., 142–143, 180 Traue, H.C., 233t, 245–246 Treasure, J., 8, 232–246, 233t, 280 Tregenza, T., 32–33 Trigg, R.E., 84t, 90, 92t Trivers, R.L., 12, 13–15 Troendle, J.F., Tronel, S., 143, 144t, 150 Tronnier, H., 199t, 207–208 Truran, D., 268t, 276, 277–278 Trussell, J., 172–173 Tsai, P.C., 233t Tschirren, B., 35, 42–43, 56t, 61t, 66–67, 77 Tsubaki, Y., 97, 98t Tumani, H., 233t, 249–250, 253t, 289 Turetsky, B.I., 168–169 Twellman, E.E., 1–2, 37, 133t, 140, 143, 144t, 150–151, 252, 292–293 Tyler, C.R., 80 Tynkkynen, K., 96–97, 101t, 113t 398   Author Index U Uchida, S., 186t Udompataikul, M., 199t, 207–208 Ulukanligil, M., 185, 186t, 205 Uno, H., 276–277 Untch, M., 233t, 289 Updegraff, J.A., 165, 175, 221, 233t, 247 Upton, M., 198 Ushijima, M., 144t Uy, J.A.C., 20–21 Uzzell, B.P., 233t V v.d Wall, E., 233t Vaccarino, V., 276 Vaillant, G.E., 278–279 Vainikka, A., 101t Valmas, M.M., 233t van Beek, Y., 176 van Bergen, E., 101t van Dam, F.S., 233t, 251 Van de Vijver, L.P., 172–173, 206–207 Van Denberg, S.G., 248–249 van der Linden, D., 225 Van Duyse, E., 37–38, 56t, 61t, 77, 79 van Elburg, T.A., 233t Van Engeland, H., 233t Van Goozen, S.H., 233t Van Horn, R.C., 29 Van Hout, A.J.M., 56t Van Iersel, J.J.A., 81 Van Noord, P.A.H., 173 Van Noordwijk, H., 44t Van Oosterhout, C., 84t, 90, 92t Van Praagh, E., 186t van Schaik, C.P., 7, 17–18, 160, 184 Van Valin, R.D., 180 Van Vugt, M., 167 Vance, E.A., 130t Vandas, G.M., 1–2, 129–139, 133t, 140, 141f, 143, 144t, 150–151, 252, 292–293 Vandenberg, S.G., 168, 289 Vandenbergh, J.G., 129, 130t, 133t, 141–142, 151–152 Vannoni, E., 133t Vanpé, C., 126t Vardy, J., Vasilyeva, M., 8, 233t, 252–261, 253t, 280–281 Vásquez, G., Vasterling, J.J., 278–279 Veenendaal, M.V., 211t Veiga, J.P., 52t Veijola, J., 226 Velando, A., 44t, 52t, 73–74 Venegas, P., 184, 185–198, 186t Venkataramani, A.S., 8, 252–260, 253t, 262–263, 280–281 Veramonti, T.L., 252 Verduijn, M.H., 5, 25–26 Vergara, P., 52t, 66–67, 73 Vergauwen, J., 56t, 61t Verhulst, S., 34–35, 52t, 66–67, 70, 72 Vermetten, E., 233t, 267, 268t Vertongen, F., 186t Vesanto, R., 211t, 253t Vicari, S., Vidrine, D.J., 252 Vieira de Castro, A.C., 56t, 61t, 77 Vigil, J., 165, 178–179, 204–205, 221, 228, 288 Vigil, J.M., 177 Vincent, A.C.J., 14, 26–27 Vishnevetsky, J., 211t, 227 Vlček, K., 250–251 Vogel, V.G., 8, 233t, 246–247, 251–252 Voigt, C.C., 133t, 139–140 vom Saal, F.S., 37, 150, 293 von dem Hagen, E., 186t, 206–207 von der Lippe, H., 225–226 von Hardenberg, A., 123–125, 126t von Helversen, O., 133t, 139–140 von Rueden, C., 162, 186t, 206, 225–226 von Schantz, T., 31, 52t, 150, 291 von Wietersheim, J., 233t, 245–246 Vora, S., 156t Voyer, D., 168, 260–261 Voyer, S., 168, 260–261 Vreugdenhil, H.J., 211t, 219–220, 219f Vrieswijk, B., 173 Vyhnálek, M., 250–251 Vythilingam, M., 233t, 267, 268t W Wachs, T.D., 186t, 253t Wack, D.S., 180 Wada, J., 166, 180, 181 Wadiwalla, M., 268t Wager, T., 169, 265–266 Wagner, H.L., 176 Wagner, L., 253t, 264 Wagner, W.E., 112, 113t Wakelin, D., 211t, 223 Walker, A., 159–160 Walker, A.R., 175 Author Index    399 Walker, D., 26–27 Walker, L.K., 44t, 71–73 Walker, R.S., 162–163, 172, 224, 225 Walker, S.P., 198, 199t Wallace, A.R., 11, 24–25, 153 Walravens, P.A., 185–198, 186t Walters, E.E., 165–166, 170, 225 Wang, A.H., 23 Wang, C., 7–8, 210–220, 211t, 219f, 253t, 286 Wang, C.H., 6, 144t Wang, J., 160–161, 186t, 203, 205, 205f, 286, 287 Wang, S.C., 130t Wang, X., 7–8, 211t, 226–227, 268t, 276 Wang, Y., 170–171 Wang, Y.M., 6, 144t, 150 Wang, Z., 160–161, 203, 268t, 276, 277–278 Wang, Z.W., 133t Ward, C.V., 159–160 Ward, K.A., 198, 285 Ward, O.B., 6, 133t, 141–142 Warzak, D.A., 1–2, 129–139, 133t, 140, 141f, 143, 150–151, 252, 292–293 Waterflow, J.C., 211t Waterreus, A., 253t, 264, 265 Watkins, W.E., 3–4, 154–155 Watson, J.B., 7–8, 211t, 226–227 Watson, N.L., 27–28 Watson, N.V., 168 Watt, G., 198 Watt, L., 1–2, 233t, 249 Waugh, C.E., 170, 266–267, 288 Wawrzyniak, G., 186t Way, A., 186t Weadick, C.J., 5–6, 89 Weaver, K., 31, 56t, 77 Weber, M., 8, 181, 233t, 246–248, 280, 286–287 Webster, L.M.I., 52t Wechsler, D., 253t, 262, 286–287 Weddle, C.B., 101t, 111 Wedekind, C., 30, 35, 42, 208, 290 Weekes-Shackelford, V.A., 155, 163, 172, 176, 231, 284–285 Wefel, J.S., 233t, 251, 252 Weihe, P., 233t, 253t Weimerskirch, H., 5–6, 56t, 76–77 Weiner, M.W., 268t, 276 Weinstock, M., 143–150, 144t, 266–267 Weisglas-Kuperus, N., 211t, 219–220, 219f Weishampel, P., 233t Weiss, D.S., 268t, 276 Weiss, P., 276 Weiss, R.E., 184, 186t, 203, 253t Weiss, S.L., 35 Weisskopf, M.G., 233t, 253t Weissman, B., 247 Welch, A.M., 5, 25–26 Welcome, S., 168–169, 180–181, 281 Welling, L.L., 199t, 206, 211t, 223 Welsh, R.C., 268t, 276 Welsh, T.H Jr, 1–2, 37, 133t, 140, 143, 144t, 150–151, 252, 292–293 Welzl, H., 143–150, 144t Weniger, G., 250–251 Wersinger, S., 166 West, K.P., 184, 186t, 203 West, P.M., 119t, 122–124, 126t, 133t Westcott, D.A., 21 West-Eberhard, M.J., 2, 12–13, 26, 27, 94, 151, 283–284 Westropp, C.K., 7, 186t Wetzel, R., 288 Weuve, J.L., 233t Whaley, S.E., 253t Wheatley, J.R., 199t, 206, 211t, 223 Wheelwright, S., 166–167, 232, 288–289 White, B.J., 221 White, C.L., 144t, 150 White, D.R., 162–163, 174 White, N.S., 180 White, P.J., 41–42, 130t White, R.F., 233t, 253t Whitehouse, P.J., 233t Whitesell, N.R., 175 Whiting, B.B., 164, 168 Wickings, E.J., 118–122, 119t, 126t Wieneke, M.H., 233t Wiesler, D., 208 Wilhelm, K., 140–141 Wilkinson, G.S., 101t, 110–111, 150–151 Williams, C.L., 143, 150 Williams, G.C., 1, 12, 13–14 Williams, L.M., 8, 267, 268t, 276, 277 Williams, M.A., 167 Williams, S.A., 1–2, 23, 24, 129–139, 133t, 140, 141f, 143, 144t, 150–151, 252, 292–293 Williamson, P., 3–4 Willis, S.L., 248–249 Wilreker, B.C., 172, 174–175, 177 Wilson, A.B., 26–27 Wilson, D., 35 Wilson, J.R., 248–249 Wilson, K., 28–29, 124–125, 126t Wilson, K.J., 13f 400   Author Index Wilson, M., 1, 163, 165–166, 170, 172, 224, 229, 246, 288 Wilson, P.W., 156t, 287 Wilson, R.S., 233t, 248–249 Winegard, B., 155, 169, 172, 176, 231, 284–285 Wingfield, J.C., 20–21, 78 Winkelser, F., 130t Winkler, A.M., 277–278 Winneke, G., 7–8, 211t, 219–220, 219f Winner, E., 232, 288–289 Winslow, D., 266 Winstead, B.A., 175 Winter, A.S., 224 Winterbotham, M., 176 Winters, S., 119t, 122–123 Wirth, M.M., 170, 266–267, 288 Witelson, S.F., 180–181 Witkin, H.A., 289 Wittsiepe, J., 7–8, 211t, 219–220, 219f Wittzell, H., 31, 150, 291 Wojcieszek, J.M., 20–21 Wolf, O.T., 253t Wolf, S., 250–251 Wolff, K., 5, 25–26 Wolgers, G., 178 Wolke, D., 9, 247 Wolters, H.J., 129–139, 133t, 151–152 Wong, B.B.M., 35, 42, 66–67, 72 Wood, B.M., 168, 264 Wood, J.A., 233t Wood, J.L., 180 Wood, W., 153–154, 284–285, 294 Woodgate, J.L., 61t, 79 Woodruff, T.K., 283 Woods, J.S., 253t, 262 Woods, R.P., 170–171, 180–181 Woolley, H.T., 153 Woon, F.L., 267 Worden, B.D., 101t World Health Organization, 284 Worthman, C.M., 173 Wouters, H., 233t Wrangham, R.W., 29, 153–154, 179 Wright, R.O., 253t Wu, F.W., 186t, 205, 205f, 286, 287 Wyatt, T.D., 125 Wyman, M.T., 133t X Xie, L., 133t, 140, 144t Xiong, W., 211t, 227 Xu, L., 144t Xu, X.H., 6, 133t, 140, 144t, 150 Xue, L., 233t Y Yamamoto, M.A.N.A.B.U., 186t Yamauchi, T., 186t, 199t Yan, A.C., 209 Yan, M., 168–169 Yanase, T., 186t Yang, C.Y., 233t Yang, J., 144t Yap, P., 186t, 205, 205f, 286, 287 Yarbrough, C., 185, 186t Yarnell, L., 179 Ye, X., 144t, 211t, 227, 286 Ye, Y.P., 6, 144t, 150 Yee, M.D., 164–165 Yehuda, R., 268t, 276 Yeo, R.A., 263–264 Yi, Q.L., 233t, 253t, 264 Yokoyama, K., 233t, 253t Yolton, K., 211t, 227, 286 Yonker, J.E., 233t Yoon, D.Y., 283 Yoshii, J., 170–171, 180–181 Young, R., 222, 279–280 Young, V., 232–246, 233t, 280 Yu, C., 186t Yuan, L., 186t, 199t Yunis, F., 186t, 253t Yusuf, S., 173 Z Zaadstra, B.M., 173 Zagron, G., 143–150, 144t Zahavi, A., 5, 12, 24–25, 30, 34, 38, 66, 81, 283–284 Zaiyouna, R., 168 Zala, S.M., 130t Zald, D.H., 180 Zanette, L., 61t, 79, 265, 291 Zann, R.A., 44t, 56t, 61t, 77, 94 Zanollo, V., 35, 44t, 52t, 74–75, 151–152 Zemel, B.S., 185–198, 186t Zervoulis, K., 210–219, 287 Zevin, J.D., 266–267 Zhang, G., 144t, 150 Zhang, J., 6, 144t, 150 Zhang, J.X., 133t Zhang, L.P., 186t, 205, 205f, 286, 287 Author Index    401 Zhang, Q., 144t, 150 Zhang, Z.B., 133t Zhao, N., 144t Zhihe, Z., 23, 24, 140 Zhou, H., 186t, 199t Zhu, C., 211t Zhu, Z., 144t Zihindula, M., 186t Zijdenbos, A., 281 Zimbron, J., 226–227 Zimmerman, I.L., 286–287 Zimmermann, M.B., 233t, 246–247, 253t Zimmermann, R.R., 142 Ziol, E.W., 233t Ziomkiewicz, A., 173 Zollinger, S.A., 56t, 61t, 77 Zonnevylle-Bender, M.J., 233t Zou, X., 144t Zrzavý, J., 160 Zucker, K.J., 222 Zuckerman, M., 224 Zuena, A.R., 143–150, 144t Zuk, M., 5–6, 24–25, 30, 33, 34–35, 38, 41–42, 44t, 52t, 56t, 72–73, 76–77, 113t Zwaan, B.J., 101t Zwitserlood, P., 265–266 Subject Index Note: Page numbers followed by f indicate figures and t indicate tables A Adolescence anxiety and depression, 165–166 childhood stressors, 162 cognitive sex differences, 166–167 heterosexual relationships, 288 mental rotation test, 289 natural language competencies, 288–289 physical changes, 161 poor nutrition, 198 social dominance and attractiveness, 164 African buffalo (Syncerus caffer), 124–125 African elephant (Loxodonta africana), 5, 129 Aggressive interactions, 29 Alpine ibex (Capra ibex), 6, 123–124, 125f, 184 Alzheimer’s disease, 1–2, 246–247, 248–249, 263–264, 265, 289 Amazonian jungle, 162–163 Ambush bug (Phymata americana), 97 American goldfinch (Spinus tristis), 5–6, 35, 66–67, 66f, 70 American kestrels (Falco sparverius), 37 American rubyspot (Hetaerina americana), 97–100, 109f Amygdala, 142–143, 169, 170, 180, 181, 227–228, 266–277 Anastrozol, 251–252 Ancylostoma braziliense, 206–207 Ancylostoma duodenale, 172–173, 205 Androgen blocking/suppressing drugs, 263–264 Anemia, 172–173, 185–198 Anna’s hummingbird (Calypte anna), 71–72, 71f Anxiety disorders, 170, 227 Arthropods behavioral traits competition and choice, 112 courtship/dominance displays, 112 drumming, 117 burrows, 96 condition-dependent behavioral traits, 113t condition-dependent color traits, 98t condition-dependent size/pattern-based traits, 101t courtship ornaments, 96 crustaceans, 96 physical traits color, 97 insects, 96–97 melanin-based colors, 96–97 parasites/pathogens, encapsulation of, 96–97 size, 97–112 Atlantic canary (Serinus canaria), 78 Australian rabbit (Oryctolagus cuniculus), 129 Australopithecines, 160–161 Australopithecus afarensis, 159–160 Australopithecus africanus, 159–160 Australopithecus anamensis, 159–160 B Bank vole (Myodes glareolus), 129 Beebe’s fiddler crab (Uca beebei), 96 Beetle See Chiasognathus grantii Onthophagus ascuminatus Behavioral vulnerabilities children’s play breastfeeding, 220–221 condition-dependent behavioral traits, humans, 211t doll play, 210–219 EDCs, 210–219 male play fighting, 210 maternal stress, 220 nutritional supplements, 220 play parenting, 210 prenatal exposure, 219–220 Pre-School Activities Inventory, 210–219 rough-and-tumble and coalitional play, 210 sex-typical play, 210, 228 sexual selection, 210 toxins, 210–219 403 404  Subject Index Behavioral vulnerabilities (Continued) risk taking and emotional composure (see Amygdala, Hippocampus) accidental injuries, 224 anxiety and depression, 225 BPA exposure, 227 enhanced risk-avoidance mechanism, women, 225 exposed and unexposed women, 226 extraversion and neuroticism, 225 harm avoidance, 226 higher-status men, 224 impulsive behavioral aggression, 225 job-related toxin exposures, 227 Kaobawä’s admonition, 224 lower-status men, 224 maltreatment, 226–227 men’s psychological ability, 225 natural stressors, 226–227 prenatal toxin exposure, 227 psychological stressors, 225–226 pubertal development, 224 solvents, 227 stress-response system, 227–228 testosterone, 227–228 social behavior coalitional play, 221 cooperative and competitive relationships, 221 dyadic friendships, 223 physical/sexual abuse, 222 same-sex social relationships, 222 sex-typical activities, 222 social adjustment, 222 social signals, 223–224 Big belly seahorse (Hippocampus abdominalis), 26–27 Bighorn sheep (Ovis canadens), 124–125 Birds behavioral traits courtship display, 76–77 developmental stressors, 77 song features and complexity, 76 brain and cognitive traits adulthood stressors, 79 age-limited song learners, 79 androgen receptors, 79–80 foraging ability, 78 HVC and RA, 79 postnatal stressors, 79 sex-specific ways, 80 song learning, 78 condition-dependent behavioral traits, 56t condition-dependent brain and cognitive traits, 61t condition-dependent color traits, 44t condition-dependent size traits, 52t nestling coloration, 42–43 organization of reviews, 43–65 physical traits color signals, types of, 66–68 conditional dependent signals, 69–72 size, 73–75 sexual selection, 43 Birdsong, 21, 22f, 31, 35, 77, 78, 80, 142–143, 266 Bisphenol A (BPA), 140, 150, 227, 292–293 Black grouse (Tetrao tetrix), 19–20, 19f, 69 Blue grosbeak (Guiraca caerulea), 68, 68f Brain and cognition, 142–150 and cognitive competition, 21–24 and cognitive traits birds, 78–80 boys and men, vulnerability, 166–171 girls and women, vulnerability, 176–181 inflammation, 150 systems, 22f vulnerabilities, 265–280 Brain vulnerabilities amygdala, hippocampus and trauma childhood maltreatment, 267 condition-dependent brain traits, humans, 268t emotion regulation system, 266–267 evolutionary approach, 267 male-male competition hypothesis, 276 prenatal and postnatal stressors, 266–267 PTSD, 267, 276 pubertal development, 266–267 stress-response system, 276 men’s condition-dependent hippocampus asocial personality, 279 childhood maltreatment, 278 environmental and social stressors, 277–278 masculinity-femininity measure, 279–280 nonveteran control groups, 277 PTSD symptoms, 279 sex-atypical behaviors, 279–280 threat detection and emotion regulation amygdala, 265–266 male-male competition, 266 men’s emotional composure, 265–266 Subject Index    405 Breast cancer, 251 Breeding season, 23, 24 Broadnosed pipefish (Syngnathus typhle), 26–27 Brown-headed cowbird (Molothrus ater), 24 Brown lemurs (Eulemur fulvus), 122–123 C California mouse (Peromyscus californicus), 1–2, 129–139, 141f, 292–293 Calopteryx haemorrhoidalis, 97 Calopteryx splendens, 97, 100f Canary (Serinus canarius), 22–23 Cardiorespiratory fitness, 205 Carotenoid-based traits, 73–74, 100–109 Cellular respiration, 31, 32, 35, 36–37, 38, 39, 290, 291, 292 CHCs See Cuticular hydrocarbons (CHCs) Chemotherapy, 251 Chiasognathus grantii, 16–17, 16f Child Activities Inventory, 287 Child Behavior Checklist, 286, 288 Child Game Participation Questionnaire, 287 Childhood abuse, 165 Childhood maltreatment, 3, 4, 267, 278–279 Childhood stressors, 155–159, 162, 171, 203 Child rearing, 175 Chimpanzee (Pan troglodytes), 140–141 Chronic stressors, 155–159, 161–162, 165–166 Cognitive deficits, 4, 250f Cognitive vulnerabilities folk physics natural stressors, 260–261 testosterone and antiandrogen therapy, 263–265 toxins, 261–263 folk psychology language, 246–252 theory of mind and emotion recognition, 232–246 Collard flycatchers (Ficedula albicollis), 74–75 Common lizards (Zootoca vivipara), 37 Compromised word learning, 251 Condition-dependent traits arthropods, 96–117 birds, 42–80 female-female competition, 41 fish, 80–91 genetic variance and inbreeding, 31–33 intrasexual competition or intersexual choice, 95 Nutritional and social stressors, 35–37 mammals, 117–150 mating partners, 41 Parasites and immunocompetence, 33–35 Toxin exposure, 37–38 Conflating stressors, 185 Corticosterone, 36–37 Cotton-top tamarin (Saguinus oedipus), 129–139 Cuticular hydrocarbons (CHCs), 110 Cyrtodiopsis dalmanni, 110–111 Cyrtodiopsis quinqueguttata, 110–111 Cyrtodiopsis whitei, 95, 110–111 D Damselfly See Hetaerina titia; Mnais costalis, Calopteryx splendens, Calopteryx haemorrhoidalis Decorated cricket (Gryllodes sigillatus), 111 Deer mice (Peromyscus maniculatus), 1–2, 37, 140, 292–293 Diamond firetails (Stagonopleura guttata), 74–75, 75f, 151–152 Diasemopsis dubia, 110–111 Diasemopsis meigenii, 5, 111 DNA fingerprinting, 18–19 Drill (Mandrillus leucophaeus), 122–123 Drosophila Montana, 112 Drosophila simulans, 95, 111 Dung beetle (Onthophagus sagittarius), 27–28, 28f E Early mortality risks, Ecological contamination, 38 EDC See Endocrine disrupting compound (EDC) Egalitarian/monogamous mating system, 18–19 Endocrine disrupting compound (EDC), 37, 80, 140, 150, 210–219, 228 Energy-demanding prenatal brain development, 291 Episodic memory, 178 European starling (Sturnus vulgaris), 31, 77 F Facial traits, 172–173 Fallow deer (Dama dama), 124–125 Family-oriented play, 175–176 406  Subject Index Fiddler crab (Uca annulipes), 96 Field cricket See Gryllus lineaticeps, Gryllus campestris Fish behavioral traits, 91 carotenoid-based color traits, 81 color traits, 80–81 condition-dependent behavioral traits, 92t condition-dependent color traits, 82t condition-dependent size/number traits, 84t deceptive signaling, 81 endocrine disrupting compounds, 80 parental investment, 81 penultimate reproductive cycle, 81 physical traits color, 89–90 size, 90–91 Fluctuating asymmetry (FA), 90 Folk physics boys and men, vulnerability, 168 visuospatial abilities, 168, 249, 250–251, 252, 260–261, 262, 263–264 cognitive traits, humans, 253t natural stressors inbreeding, 260 mazes test, 260 sentence comprehension test, 260–261 sex- and trait-specific effects, 260 socioeconomic status, 260–261 spatial reasoning ability, 260 verbal fluency test, 260 predicted condition-dependent traits in humans, 156t route learning, 252–260 spatial drawing test, 249 spatial learning and memory, 23, 143–150, 293 spatial navigation, 1–2, 23, 292 testosterone and antiandrogen therapy antiandrogen treatment, 264 block design/mental rotation tests, 265 block design task, 264 prostate cancer, 263–264 route-learning task, 264 spatial cognition tasks, 265 visuospatial tasks, 264 word learning, 264 toxins cocaine, 263 dose-response assessment, 262 environmental toxins, 262 malaria eradication study, 262–263 spatial ability test, 262 visual memory and attention, 261–262 visual memory and attention deficits, 262 word learning and verbal memory, 262 Folk psychology boys and men, vulnerabilty, 167–168 language Alzheimer’s disease, 246–247, 248–249 chemotherapy, 251 premature birth, 247 theory of mind and emotion recognition Alzheimer’s disease, 248–251, 252 anorexia nervosa, 232 bulimia, 245–246 cognitive traits, humans, 233t emotion cues, 245–246 emotion recognition tests, 232 facial expressions, 245–246 facial features, 245–246 female-female competition, 246 intelligence, 232–245 physical-state inferences, 232–245 predicted condition-dependent traits in humans, 156t reproductive competition, 246 sex-specific sensitivity, 246 social cognition deficits, 232–245, 245f vocal intonation, 245–246 Fossil record, 159–160 Frigate bird (Fregata magnificens), 5–6, 76–77, 76f Fruit fly See Drosophila Montana, Drosophila simulans G Gelada baboon (Theropithecus gelada), 122–123, 123f Golden hamster (Mesocricetus auratus), 41–42, 129 Gonorrhea (Neisseria gonorrhoeae), 209 Good genes models, 24–25 Gorillas (Gorilla gorilla), 160 Grass butterfly (Eurema hecabe), 97 Gray tree frog (Hyla versicolor), 25–26 Great tit (Parus major), 37–38, 42–43, 74, 74f Gryllus campestris, 6, 112, 291 Gryllus lineaticeps, 112 Guppy (Poecilia reticulata), 5–6, 80, 89f, 290–291 H Hetaerina titia, 100–109 Higher/high vocal center (HVC), 21–22, 79–80 Hihi (Notiomystis cincta), 72–73 Subject Index    407 Hippocampus, 6, 8, 23, 24, 31, 78, 143, 150, 169, 170, 265–280 Homo erectus, 159–160 Homo ergaster, 159–160 Hookworm See Ancylostoma braziliense, Ancylostoma duodenale, Necator americanus House finch (Carpodacus mexicanus), 34, 290–291 House sparrow (Passer domesticus), 72–73 Huia (Heteralocha acutirostris), 12–13, 13f Human health and development molecular mechanisms, 283 natural selection, 283–284 sex differences, 283 stressors environmental toxins, 289–290 natural stressors, 290–292 therapeutic toxins, 289–290 toxins, 292–293 well-being and vulnerability adults, 289 age-appropriate measures, 285–286 disease, developmental origins of, 285 parental treatment/social opportunity, 284–285 preschool children, 286–287 schistosomiasis, 285 school-age children and adolescents, 287–289 sex-specific norms, 284 stressors, 285 WHO, 284 Human neocortex, 171f Human vulnerability behavioral vulnerabilities, 209–228 brain vulnerabilities, 265–280 condition-dependent behavioral traits in humans, 211t condition-dependent brain traits in humans, 268t condition-dependent physical traits in boys and men, 186t condition-dependent physical traits in girls and women, 199t condition-dependent folk physics cognitive traits in humans, 253t condition-dependent folk psychological cognitive traits in humans, 233t cognitive vulnerabilities, 232–265 folk physics competencies, 231 Kaobawä’s admonition, 231–232 physical vulnerabilities, 184–209 predicted condition-dependent traits in humans, 156t relational aggression, 231 sex-specific vulnerabilities, 183 I Illinois Test of Psycholinguistic Abilities, 286–287, 288–289 Immune system competence, 69 Immunocompetence handicap hypothesis, 33 Impulsive aggression, 288 Inbreeding depression, 32 Internal gestation, 14–15 Intestinal worms (Trichostrongylus tenuis), 34 J Japanese macaque (Macaca fuscata), 15 Junco (Junco hyemalis), 74–75 K Kudu (Tragelaphus strepsiceros), 16–17, 17f L Language Alzheimer's disease, 248–251, 252 basics skills and relational, aggression, 180-181 condition-dependent folk psychological cognitive traits in humans, 233t premature birth, 246–247 Lateral magnocellular nucleus of the nidopallium (LMAN), 21–22 Leafy seadragon (Phycodurus eques), 26–27 Lekking species, 19–20 Lion (Panthera leo), 122–123 M Macaca sylvanus, 151–152 Macaca mulatta, 122–123 Malaria (Plasmodium vivax), 260 Male vulnerability, 3–4 Mammals behavioral pheromone communication, 125 scent, 125–129 brain and cognition, 142–150 condition-dependent behavioral traits, 129–142, 133t condition-dependent brain and cognitive traits, 144t 408  Subject Index Mammals (Continued) condition-dependent color traits, 119t condition-dependent size traits, 126t physical color, 117–123 size, 123–125 Mandrill (Mandrillus sphinx), 95, 117–118, 118f Marmoset (Callithrix jacchus), 129, 139f, 161, 291 Mate-search strategy, 140 Maze and route learning, 250–251 Meadow vole (Microtus pennsylvanicus), 23, 140, 168 Melanin-based trait, 100–110 Melanin pigments, 67–68 Milky fiddler crab (Uca lacteal), 96 Mnais costalis, 97, 100f Mortality risks, 32–33 Mosquito fish (Gambusia holbrooki), 37 Mouse (Mus musculus), 95, 292 N Necator americanus, 172–173, 205 Nesting sites, 15–17 Nestlings, 66–67 Neuropsychological test batteries, 289 Nonverbal behavior, decoding, 176–177 Northern elephant seal (Mirounga angustirostris), 17–19, 18f, 123–124, 159–160 Norway rat (Rattus norvegicus), 140–141 Nutritional stressors, 292 O Obligatory postpartum female care, 14–15 Onthophagus ascuminatus, 111 Operational sex ratio (OSR), 14, 15–16 Oxidative stress, 150 See also Cellular respiration P Paper wasp (Polistes dominulus), 6, 109–110, 109f Parasite (Toxoplasma gondii), 142, 226 Parasitic infections, 172–173 Parasitic worm (Onchocerca volvulus), 207–208 Parental investment, 13–14, 26 Peacock (Pavo cristatus), 5, 25–26 Peafowl (Pavo cristatus), 25f Pheromones, 125–129 Physical dominance, 175–176 Physical vulnerabilities, human condition-dependent physical traits, 184 in boys and men, 186t in girls and women, 199t muscle mass and fat reserves childhood stressors, 203 fat reserves, 203 high vs low food availability, 204 poor nutrition, 203 skeletal development developmental stressors, 184 facial features and skin attractiveness, 206–208 height, 185–198 pelvic development, 198–202 physical fitness and activity, 204–205 pubertal development, 184 scent and health, 208–209 socioeconomic status, 184 Pied flycatchers (Ficedula hypoleuca), 77 Play fighting, 125, 141–142 See also Roughand-tumble play Plumage coloration, 66–67 Polychlorinated biphenyls (PCBs), 262–263 Post-traumatic stress disorder (PTSD), 8, 267 Prairie voles (Microtus ochrogaster), 23 Predator alarms, 139–140 Pre-School Activities Inventory, 286 Progressive matrices test, 260 Projectile weapons, 168 Prosody, 178 PTSD See Post-traumatic stress disorder (PTSD) R Rat (Rattus norvegicus), 6, 37, 171, 292 Real-world routes, 250–251 Red deer (Cervus elaphus), 95, 123–124, 124f, 184, 291 Red grouse (Lagopus lagopus), 34, 73 Red jungle fowl (Gallus gallus), 5–6, 41–42, 66–67, 67f Red kangaroos (Macropus rufus), 140–141 Red-necked phalarope (Phalaropus lobatus), 27 Relational aggression, 173–174, 248 Reproductive rate hypothesis, 26 Ring-tailed lemur (Lemur catta), 129 Robustus arcopallium (RA), 21–22 Rough-and-tumble play, 204–205, 210, 220, 221, 222 See also Play fighting Roughhousing, 164 Subject Index    409 S Sac-winged bat (Saccopteryx bilineata), 139–140 Sand pillars, 96 Satin bowerbird (Ptilonorhynchus violaceus), 20, 20f Scent-marking behavior, 129 Schistosomiasis (Schistosoma mansoni), 285 School-taught academic abilities, 166 Scramble competition, 23 Sedge warbler (Acrocephalus schoenobaenus), 78 Sex-role reversed species, 26 Sex-specific vulnerabilities hypothesis boys and men adolescence, 155–159 behavioral traits, 162–166 brain and cognitive traits, 166–171 childhood stressors, 155–159 chronic stressors, 155–159 condition-dependent traits, humans, 156t condition-dependent physical traits in boys and men, 186t physical traits, 159–162 stress exposure, 155 girls and women arranged marriages, 172 behavioral traits, 173–176 brain and cognitive traits, 176–181 condition-dependent traits, humans, 156t condition-dependent physical traits in girls and women, 199t free choice marriages, 172 physical traits, 172–173 polygynous marriages, 172 natural selection, 153 operational sex ratio, 153–154 social and social-cognitive processes, 153–154 socially imposed monogamy, 153–154 Sexual selection associated vulnerability, 12 competition for mates/mate choice operational sex ratio, 15–16 reproduction, rate of, 14–15 condition-dependent traits behavioral traits, 30–31 behavioral traits in arthropods, 113t behavioral traits in birds, 56t behavioral traits in fish, 92t behavioral traits in humans, 56t behavioral traits in mammals, 133t brain and cognitive traits in birds, 61t brain and cognitive traits in mammals, 144t brain traits in humans, 268t cellular respiration, 31, 32, 35, 36–37, 38, 39 color traits in arthropods, 98t color traits in birds, 44t color traits in fish, 82t color traits in mammals, 119t costly signals, 30 critical brain functions and cognitive competencies, 31 disease resistance vs nutritional status, 30 early nutritional/social stressors, 31 folk physics cognitive traits in humans, 253t folk psychology cognitive traits in humans, 233t genetic variance and inbreeding depression, 31–33 nutritional and social stressors, 35–37 parasites and immunocompetence, 33–35 physical traits in boys and men, 186t physical traits in girls and women, 199t plumage color, 30–31 scent traits in mammals, 84t size or number traits in fish, 84t size or pattern-based traits in arthropods, 101t size traits in birds, 52t size traits in mammals, 82t toxins, 37–38 cross-generational changes, 11 female choice, 24–26 female-female competition and male choice female-female competition and social selection, 27–29 male choice, 29 reversed sex roles, 26–27 intersexual choice, 11 intrasexual competition, 11 male-male competition behavioral competition, 19–21 brain and cognitive competition, 21–24 physical competition, 17–19 parenting, 12 sex differences, 12 sex-role reversed species, 12 Shape memory test, 249–250 Skeletal development developmental stressors, 184 facial features and skin attractiveness carotenoids, 206–207 dietary carotenoid levels, 207 410  Subject Index Skeletal development (Continued) facial and physical attractiveness, 206–207 hormone profiles, 206 human skin color, 207 low- and high-flavanol, 207–208 pubertal development, 206 skin lesions, 206–207, 206f women’s marriage prospects, 208 height condition-dependent physical traits, boys and men, 186t poor nutrition/low SES, 185 premature death, 198 short stature, 198 zinc supplementation, 185–198 pelvic development compromised height, 198 condition-dependent physical traits, girls and women, 199t low SES family, 202 parasite levels, 202 poor nutrition, 198 pubertal development, 184 scent and health disease-specific VOCs, 209 infectious disease, 209 innate immune response, 209 lung cancer, 209 natural scents, 208 odors, use of, 209 oxidative stress, 209 pheromones, 208 sex-specific VOC/odor cues, 208 tuberculosis, 209 Sneaking, 18–19 Soay sheep (Ovis Aries), 28–29, 124–125 Social dominance, 122–123, 292–293 Social exclusion, 179 Social learning, 20–21 Social selection, 27–29 Socioeconomic status (SES), 184, 260–261 Sociometric analysis, 288 Song sparrow (Melospiza melodi), 78, 291 Southern elephant seal (Mirounga leonina), 17–18 Spanish pond turtle (Mauremys leprosa), 35 Spatial abilities See Folk physics Sphyracephala beccarri, 110–111 Spotted hyena (Crocuta crocuta), 140–141 Stalk-eyed flies (Diopsidae) See Cyrtodiopsis whitei; Diasemopsis meigenii; Diasemopsis meigenni Stickleback (Gasterosteus aculeatus), 5, 41–42, 80 Stoat (Mustela ermine), 151–152 Stress hormone, 36–37 Stress regulation, 169f Striped plateau lizard (Sceloporus virgatus), 35 Swamp sparrow (Melospiza georgiana), 77 T Tamoxifen, 251–252 Tangshan earthquake, 226–227 Teleopsis quadriguttata, 110–111 Temperament and Character Inventory, 288 The Eyes Test, 288–289 The Hornet’s, 154f Theory of mind, 178–179, 232 Thick-legged fiddler crab (Uca crassipes), 96, 96f Trail-and-error learning, 21–22 Tsimane (Amazonian horticulturalists), 225–226 Two-spotted goby (Gobiusculus flavescens), 15–16 V Vervet (Cercopithecus aethiops), 122–123, 122f Vinclozolin, 141–142 Virtual maze tests, 250–251 Visuospatial abilities, 252 Visuospatial competencies, 292 Vocal communication, 21 Volatile organic compounds (VOCs), 208 Vulnerability competitive ability, cross-species vulnerabilities, environmental toxins and chemotherapy, evolutionary perspective, 3–4 human vulnerabilities maltreatment, 7–8 men’s emotional composure, nutritional deficits and disruptions, physical vulnerabilities, prenatal exposure, toxins, 7–8 PTSD, social-cognitive competencies, language competencies, women, 1–2 male-on-male aggression, nonhuman vulnerabilities arthropods, cheating, competitive advantages, Subject Index    411 developmental stressors, evolutionary conservation, 5–6 parasites, poor immune system, poor postnatal nutrition, prenatal exposure, spatial-navigational abilities, vigorous behavioral displays, reckless driving, reproductive traits, timing, 1–2 sex- and species-specific traits, W Waist-to-hip ratio (WHR), 173 Wallace, 24–25 Waltzing fly (Prochyliza xanthostoma), 111–112 Water strider (Gerris incognitus), 111 Wechsler Preschool and Primary Scale of Intelligence, 286–287 White-crowned sparrows (Zonotrichia leucophrys), 77 WHO See World Health Organization (WHO) Wolf spider (Hygrolycosa rubrofasciata), 6, 117 Women’s cognitive competencies, 251–252 Woodland voles (Microtus pinetorum), 23 Word learning and memory, 249–250, 251–252 Working memory, 249–250 World Health Organization (WHO), 284 Y Yanomamö, 162–163 Yellow baboons (Papio cynocephalus), 139–140 Yellow-legged gulls (Larus michahellis), 73–74 Z Zahavi’s handicap hypothesis, 34 Zebra finch (Taeniopygia guttata), 5–6, 31, 36f, 73–74 Zebra fish (Danio rerio), 37 ... directly for mates or choose among them is tightly linked to parenting Choosiness increases with increases in investment in offspring, and competitiveness increases with decreases in investment in offspring... differences in physical and behavioral vulnerabilities in Chapter 6 and in brain and cognitive vulnerabilities in Chapter 7 Implications for understanding and studying the nuances of human vulnerabilities... experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein In using such information or methods they should be mindful of their own safety and