David Crews

Last updated
David Crews
David Crews Fishing.jpg
Born
David Pafford Crews

Jacksonville, Florida, U.S.
Alma mater The University of Maryland, Rutgers University
Known forAnimal behavior, reproductive behavior, sexual differentiation, neuroendocrinology and translational epigenetics
Scientific career
Fields Psychology, zoology, animal behavior
Institutions The University of Texas at Austin
Doctoral advisor Daniel S. Lehrman, Jay S. Rosenblatt

David Pafford Crews is the Ashbel Smith Professor of Zoology and Psychology at the University of Texas at Austin. He has been a pioneer in several areas of reproductive biology, including evolution of sexual behavior and differentiation, neural and phenotypic plasticity, and the role of endocrine disruptors on brain and behavior.

Contents

Biography

Crews enrolled at the Munich campus of the University of Maryland in 1965, then transferred to the College Park campus in 1967. [1] He graduated with a B.A. (Psychology and Sociology majors) in 1969. Following a summer as a research assistant at Walter Reed Army Institute of Research in the Department of Experimental Psychology he decided to pursue a degree in psychology. [1] Crews received a Ph.D. in Psychobiology as a National Institute of Mental Health Predoctoral Trainee at the Institute of Animal Behavior at Rutgers University in 1973 under the mentorship of Daniel S. Lehrman and Jay S. Rosenblatt.

He completed a National Science Foundation Postdoctoral Fellowship mentored by Paul Licht at the Department of Integrative Biology at the University of California, Berkeley until 1975. [1] He was then appointed as a lecturer in the Departments of Biology and Psychology at Harvard University. He was promoted to assistant professor in 1976 and to associate professor in 1979. While at Harvard he was also an associate at the Museum of Comparative Zoology. In 1982, he joined the faculty of the Department of Zoology (now Integrative Biology) at the University of Texas at Austin, where he became the Ashbel Smith Professor of Zoology and Psychology in 1998. [1]

Research

Origin of sexual behavior

Crews has argued that the primary function of sexual behavior, namely the stimulation and coordination of the reproductive physiologies of the interacting individuals (usually male and female), originated with the first unicellular organisms and hence predates the evolution of sexual recombination. He has challenged the Organizational/Default doctrine of sex determination, extending it to sexual differentiation of the brain and arguing for its replacement with an Ancestral (female)/Derived (male) paradigm. This concept has led to questions such as why might males be more like females than females are like males? The utility of this concept is becoming apparent as we continue to gather evidence for gender differences in genetic and mental disorders. He also has been a major player in the area of the evolution and diversity of steroid hormone receptors. [2] [3] [4]

Red-sided Garter

Crews discovered the important principle that sexual behavior, gamete production, and steroid hormone secretion could be dissociated, in his studies of the red-sided garter snake (T. s. parietalis). These snakes are the northernmost reptile and hibernate for much of the year, responding to temperature both to emerge from winter dormancy and to engage in sexual behavior. It was his work with this species that provided the first demonstration that the activation of sexual behavior could be independent of sex steroid hormones, depending instead upon increasing spring temperature. This work also led to the first isolation, identification and synthesis of a new class of pheromones. [5]

Whiptail Lizard

The desert grassland whiptail lizard (A. uniparens), presented an opportunity to study first-hand how the neuroendocrine substrates underlying sexual behavior can evolve. In this instance, Crews used a parthenogenetic species derived from interbreeding of two sexual species. Remarkably, although the descendant species consists only of females, reproducing by obligate parthenogenesis, individuals continue to display sexual behaviors that are typical of both females and males, alternating behaviors depending upon their individual hormone profiles across reproductive cycles. Although it is not immediately apparent what benefit could come of females engaging in male-typical behaviors in a parthenogenetic species, Crews has shown that this behavior is important to stimulate reproduction of both individuals in these pairings. [6]

By comparing the unisexual descendants with their sexual ancestors, Crews revealed how hormone-brain controlling mechanisms evolve. This work led to the examination of how novel hormone-brain controlling mechanisms might respond to new challenges. Of particular note is the revelation that the male-typical sexual behaviors which parthenogenetic females display turn out to be under the control of the postovulatory surge of progesterone rather than androgen, which the parthenogens do not produce. This discovery in the parthenogenetic lizard led Crews to extend his work to genetically modified mice and rats, demonstrating that progesterone is not a “female-specific” hormone but plays a critical role in sexual behavior in males. Indeed, Crews demonstrated that androgen and progesterone synergize in males to control copulatory behavior much as estrogen and progesterone synergize in females to facilitate sexual receptivity. These discoveries have shed light on recent work in humans suggesting a clinical significance of progesterone in male sexual behavior.

Temperature-dependent sex determination

Crews has been the leader in determining the physiological and molecular bases of temperature-dependent sex determination (TSD). Sex determination is a case study in how evolution has produced different mechanisms for achieving the same end. In many reptiles the sex of the offspring depends on the incubation temperature of the egg, not on genotype as in mammals. One question concerns how the physical stimulus of temperature is transduced into a molecular and physiological stimulus to determine an individual's gonadal sex. Crews demonstrated that incubation temperature acts on a group of genes homologous to those in mammals that affect gonadal differentiation. [7] This work helped overturn the classic tenet that males are the “organized” sex and females the “default” sex. Today we recognize both sexes as organized and the question now becomes how the activation of a conserved network of genes leads to a binary response (ovary or testis).

Leopard Gecko

He is a pioneer in the relatively new field (actually rebirth) of phenotypic plasticity, or the process by which the environment induces different phenotypes from a given genotype. When considering that species without sex chromosomes possess all of the genes necessary to develop the phenotype of both sexes, it becomes apparent that the process of sex determination and sexual differentiation represents a form of phenotypic plasticity. Using the leopard gecko (E. macularius) as the animal model system, Crews determined how the experience of temperature during a narrowly defined period of embryogenesis affects the total phenotype of the adult organism, accounting for much of the variation observed among individuals in morphology, growth, endocrinology, neural activity, and neuroanatomy. [8] [9] Some sociosexual behaviors and brain measures are affected directly by incubation temperature, whereas both incubation temperature as well as gonadal sex influences others.

Epigenetics

Crews was the first to demonstrate that behavioral differences among genetically modified mice may be exaggerated or blurred by the postnatal environment. For example, mice develop in litters of varying sex ratios and genotypes, and it is possible that some of the diagnostic behavioral characteristics may result from an interaction of the sex ratio and genotype ratio of the litter. By varying sex ratios and genotypes, he was able to show that the diagnostic behavioral characteristics and their underlying neural activity result from an interaction of sex and genotype ratio of the litter. [10] This type of work calls attention to the need for researchers using genetically modified animal models to consider the context in which the phenotypes emerge.

Transgenerational epigenetics

Crews discovered that the transgenerational epigenetic modification caused by vinclozolin exposure changes the way rats three generations removed (F3) from the original exposure perceive and react to conspecifics. [11] This was the first demonstration that endocrine disrupting chemicals (EDCs) can promote a transgenerational alteration in the epigenome that influences sexual selection, and possibly affect the viability of a population and evolution of the species. This work was recognized by the University Cooperative Society with the 2008 Research Excellence Award for Best Research Paper, University of Texas at Austin, [12] and was listed as one of the "Top 100 Science Stories of 2007" by Discover Magazine . [13] Crews then extended his work into the realm of social, learning, and anxiety-related behaviors as well as the functional activity of the brain mechanisms that underlie them. His most recent work demonstrated that ancestral exposure to EDCs alters how descendants perceive and react to life challenges, in this case stress experienced during adolescence. [14] [15] Specifically, he established that environmentally induced epigenetic transgenerational inheritance alters brain development and genome activity to modify stress-induced behavioral responses exhibited by F3 males. [16] [17] This latest work has been hailed as "important paper and a paradigm shift in our understanding of the interaction between epigenetic change and behaviors." [18]

Crews also explored the theoretical aspects of environmental epigenetics, making the important distinction between the nature of epigenetic modifications. Context-dependent epigenetic change occurs as a consequence of exposure. A defining element is that this type of change requires continued exposure to the environmental insult. For example, environmental factors that bring about an epigenetic modification may simply continue to persist. Should the diet, behavior, or a toxic environmental exposure continues across generations, the epigenetic modification will manifest in each generation. Such environmentally induced epigenetic state(s) can be reversed by removal or alteration of the factor, addition of a different environmental factor, or emigration from the contaminated site. Another form of epigenetic modification may occur when the change in the epigenome is incorporated into the germline, a process Crews has termed germline-dependent epigenetic change. In this type, the effect manifests in each generation even in the absence of the causative agent. Context-dependent epigenetic modification is fundamentally different from germline-dependent epigenetic modification. Although both have been attributed with “transgenerational” properties, only in the latter (germline) instance will the trait be passed to the next generation even in the absence of any continued exposures or stimuli. Taken together this work has generated a new perspective on the old question of ‘inherited vs experienced, ancestral vs acquired, or nature vs nurture’ and promises to shed new light on health management strategy. [19]

Environmental issues

With Andrea Gore of the University of Texas at Austin, College of Pharmacy, Crews has explored the reality of living in a contaminated world. [20] They showed that the links between nature and nurture need to be redefined to accommodate anthropogenic chemical contamination. In recognizing and accepting this worldwide change, the types of adaptations that have occurred as a consequence must be considered. In addition, they proposed a fundamental shift in the field that integrates various disciplines involved in the study of environmental contamination to recognize that contamination is widespread and cannot be remedied at the global level. Thus, greater effort must be placed on integrative and interdisciplinary studies that explicitly illuminate how the causal mechanisms and functional outcomes of related processes operate at each level of biological organization while at the same time revealing the relations among the levels. This article caused a good deal of comment, and with analysis now extending to the problem of evolution in a contaminated world. [21] Here they discuss how epigenetic outcomes at the level of both the individual organism and the evolution of the population has created ‘new species’.

Crews founded Reptile Conservation International in 1992 based on his discovery that application of estrogen to turtle and gecko eggs skews the sex distribution toward females. [22] They have been able to use this discovery to increase numbers of breeding females for three species of threatened reptile. [22]

Educational impact

Crews has had a significant impact on science and our understanding of nature. Introductory textbooks in biology, psychology, ecology, evolution, and neuroscience use his work to illustrate various principles; indeed his work has penetrated to the high school textbook level. His work is also frequently seen in film and television programs and has been featured in several articles and texts in the philosophy of science (e.g., Writing Biology by Greg Myers). Lastly, he has played a major role in the mentoring of undergraduates in research, many of whom have gone on to research in medicine and various academic careers. This mainly has been via a vehicle of his own making, the Undergraduate Biomedical Training Program, initiated while he was at Harvard University and continued to this day at the University of Texas at Austin. [23] This program has graduated over 54 students, many of whom are active researchers today, and produced more than 80 original papers with the students as authors, in many cases as first author.

Honors and awards

Selected publications

Crews has published over 400 papers, [24] with 5 papers in Nature, 9 papers in Science, 8 papers in the Proceedings of the National Academy of Sciences of the United States of America , and 4 papers in Scientific American ; and edited 4 books.

Related Research Articles

<span class="mw-page-title-main">Heredity</span> Passing of traits to offspring from the species parents or ancestor

Heredity, also called inheritance or biological inheritance, is the passing on of traits from parents to their offspring; either through asexual reproduction or sexual reproduction, the offspring cells or organisms acquire the genetic information of their parents. Through heredity, variations between individuals can accumulate and cause species to evolve by natural selection. The study of heredity in biology is genetics.

<span class="mw-page-title-main">Sex-determination system</span> Biological system that determines the development of an organisms sex

A sex-determination system is a biological system that determines the development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two common sexes and a few less common intersex variations.

<span class="mw-page-title-main">Biology and sexual orientation</span> Field of sexual orientation research

The relationship between biology and sexual orientation is a subject of on-going research. While scientists do not know the exact cause of sexual orientation, they theorize that it is caused by a complex interplay of genetic, hormonal, and environmental influences. However, evidence is weak for hypotheses that the post-natal social environment impacts sexual orientation, especially for males.

<span class="mw-page-title-main">Hypothalamus</span> Area of the brain below the thalamus

The hypothalamus is a small part of the brain that contains a number of nuclei with a variety of functions. One of the most important functions is to link the nervous system to the endocrine system via the pituitary gland. The hypothalamus is located below the thalamus and is part of the limbic system. It forms the ventral part of the diencephalon. All vertebrate brains contain a hypothalamus. In humans, it is the size of an almond.

<span class="mw-page-title-main">Sexual dimorphism</span> Condition where males and females exhibit different characteristics

Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, particularly characteristics not directly involved in reproduction. The condition occurs in most dioecious species, which consist of most animals and some plants. Differences may include secondary sex characteristics, size, weight, color, markings, or behavioral or cognitive traits. Male-male reproductive competition has evolved a diverse array of sexually dimorphic traits. Aggressive utility traits such as "battle" teeth and blunt heads reinforced as battering rams are used as weapons in aggressive interactions between rivals. Passive displays such as ornamental feathering or song-calling have also evolved mainly through sexual selection. These differences may be subtle or exaggerated and may be subjected to sexual selection and natural selection. The opposite of dimorphism is monomorphism, when both biological sexes are phenotypically indistinguishable from each other.

<span class="mw-page-title-main">Sexual differentiation</span> Embryonic development of sex differences

Sexual differentiation is the process of development of the sex differences between males and females from an undifferentiated zygote. Sex determination is often distinct from sex differentiation; sex determination is the designation for the development stage towards either male or female, while sex differentiation is the pathway towards the development of the phenotype.

Sex differences in psychology are differences in the mental functions and behaviors of the sexes and are due to a complex interplay of biological, developmental, and cultural factors. Differences have been found in a variety of fields such as mental health, cognitive abilities, personality, emotion, sexuality, friendship, and tendency towards aggression. Such variation may be innate, learned, or both. Modern research attempts to distinguish between these causes and to analyze any ethical concerns raised. Since behavior is a result of interactions between nature and nurture, researchers are interested in investigating how biology and environment interact to produce such differences, although this is often not possible.

<span class="mw-page-title-main">Vinclozolin</span> Fungicide used on fruits and vegetables

Vinclozolin is a common dicarboximide fungicide used to control diseases, such as blights, rots and molds in vineyards, and on fruits and vegetables such as raspberries, lettuce, kiwi, snap beans, and onions. It is also used on turf on golf courses. Two common fungi that vinclozolin is used to protect crops against are Botrytis cinerea and Sclerotinia sclerotiorum. First registered in 1981, vinclozolin is widely used but its overall application has declined. As a pesticide, vinclozolin is regulated by the United States Environmental Protection Agency. In addition to these restrictions within the United States, as of 2006 the use of this pesticide was banned in several countries, including Denmark, Finland, Norway, and Sweden. It has gone through a series of tests and regulations in order to evaluate the risks and hazards to the environment and animals. Among the research, a main finding is that vinclozolin has been shown to be an endocrine disruptor with antiandrogenic effects.

<span class="mw-page-title-main">Marc Breedlove</span>

Stephen Marc Breedlove is the Barnett Rosenberg professor of Neuroscience at Michigan State University in East Lansing, Michigan. He was born and raised in the Ozarks of southwestern Missouri. After graduating from Central High School in 1972, he earned a bachelor's degree in Psychology from Yale University in 1976, and a Ph.D. in psychology from UCLA in 1982. He was a professor of psychology at the University of California, Berkeley from 1982 to 2003, moving to Michigan State in 2001. He works in the fields of Behavioral Neuroscience and Neuroendocrinology. He is a member of the Society for Neuroscience and the Society for Behavioral Neuroendocrinology, and a fellow of the Association for Psychological Science (APS) and the Biological Sciences section of the American Association for the Advancement of Science (AAAS).

<span class="mw-page-title-main">Temperature-dependent sex determination</span> Environmental sex determination by temperature during development

Temperature-dependent sex determination (TSD) is a type of environmental sex determination in which the temperatures experienced during embryonic/larval development determine the sex of the offspring. It is observed in reptiles and teleost fish, with some reports of it occurring in species of shrimp. TSD differs from the chromosomal sex-determination systems common among vertebrates. It is the most studied type of environmental sex determination (ESD). Some other conditions, e.g. density, pH, and environmental background color, are also observed to alter sex ratio, which could be classified either as temperature-dependent sex determination or temperature-dependent sex differentiation, depending on the involved mechanisms. As sex-determining mechanisms, TSD and genetic sex determination (GSD) should be considered in an equivalent manner, which can lead to reconsidering the status of fish species that are claimed to have TSD when submitted to extreme temperatures instead of the temperature experienced during development in the wild, since changes in sex ratio with temperature variation are ecologically and evolutionally relevant.

<span class="mw-page-title-main">Environmental sex determination</span> Method of sex-determination

Environmental sex determination is the establishment of sex by a non-genetic cue, such as nutrient availability, experienced within a discrete period after fertilization. Environmental factors which often influence sex determination during development or sexual maturation include light intensity and photoperiod, temperature, nutrient availability, and pheromones emitted by surrounding plants or animals. This is in contrast to genotypic sex determination, which establishes sex at fertilization by genetic factors such as sex chromosomes. Under true environmental sex determination, once sex is determined, it is fixed and cannot be switched again. Environmental sex determination is different from some forms of sequential hermaphroditism in which the sex is determined flexibly after fertilization throughout the organism’s life.

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<span class="mw-page-title-main">Environment and sexual orientation</span> Field of sexual orientation research

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<span class="mw-page-title-main">Prenatal hormones and sexual orientation</span> Hormonal theory of sexuality

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<span class="mw-page-title-main">Transgenerational epigenetic inheritance</span> Epigenetic transmission without DNA primary structure alteration

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The ovulatory shift hypothesis holds that women experience evolutionarily adaptive changes in subconscious thoughts and behaviors related to mating during different parts of the ovulatory cycle. It suggests that what women want, in terms of men, changes throughout the menstrual cycle. Two meta-analyses published in 2014 reached opposing conclusions on whether the existing evidence was robust enough to support the prediction that women's mate preferences change across the cycle. A newer 2018 review does not show women changing the type of men they desire at different times in their fertility cycle.

Ecological evolutionary developmental biology (eco-evo-devo) is a field of biology combining ecology, developmental biology and evolutionary biology to examine their relationship. The concept is closely tied to multiple biological mechanisms. The effects of eco-evo-devo can be a result of developmental plasticity, the result of symbiotic relationships or epigenetically inherited. The overlap between developmental plasticity and symbioses rooted in evolutionary concepts defines ecological evolutionary developmental biology. Host- microorganisms interactions during development characterize symbiotic relationships, whilst the spectrum of phenotypes rooted in canalization with response to environmental cues highlights plasticity. Developmental plasticity that is controlled by environmental temperature may put certain species at risk as a result of climate change.

<span class="mw-page-title-main">Arthur P. Arnold</span> American biologist

Arthur Palmer Arnold is an American biologist who specializes in sex differences in physiology and disease, genetics, neuroendocrinology, and behavior. He is Distinguished Professor of Integrative Biology & Physiology at the University of California, Los Angeles (UCLA). His research has included the discovery of large structural sex differences in the central nervous system, and he studies of how gonadal hormones and sex chromosome genes cause sex differences in numerous tissues. His research program has suggested revisions to concepts of mammalian sexual differentiation and forms a foundation for understanding sex difference in disease. Arnold was born in Philadelphia.

References

  1. 1 2 3 4 "David Crews Curriculum Vitae". The Reproductive Biology Laboratory of David Crews. The University of Texas at Austin. Retrieved 18 April 2016.
  2. ↑ Crews, David (1979). "The hormonal control of behavior in a lizard". Scientific American. 241 (2): 180–187. Bibcode:1979SciAm.241b.180C. doi:10.1038/scientificamerican0879-180. PMID   493916.
  3. ↑ Crews, David; Moore, Michael C. (1986). "Evolution of mechanisms controlling mating behavior". Science. 231 (4734): 121–125. Bibcode:1986Sci...231..121C. doi:10.1126/science.3941893. PMID   3941893.
  4. ↑ Crews, David (1994). "Animal sexuality". Scientific American. 270 (1): 108–114. Bibcode:1994SciAm.270a.108C. doi:10.1038/scientificamerican0194-108. PMID   8284656.
  5. ↑ Crews, David; Garstka, William R. (1982). "The Ecological Physiology of a Garter Snake". Scientific American. 247 (5): 158–168. Bibcode:1982SciAm.247e.158C. doi:10.1038/scientificamerican1182-158.
  6. ↑ Crews, David (1987). "Courtship in unisexual lizards: A model for brain evolution". Scientific American. 257 (6): 116–121. Bibcode:1987SciAm.257f.116C. doi:10.1038/scientificamerican1287-116.
  7. ↑ Shoemaker, Christina M.; Crews, David (2009). "Analyzing the coordinated gene network underlying temperature-dependent sex determination in reptiles". Seminars in Cell & Developmental Biology. 20 (3): 293–303. doi:10.1016/j.semcdb.2008.10.010. PMC   2729108 . PMID   19022389.
  8. ↑ Gutzke, William H.; Crews, David (1988). "Embryonic temperature determines adult sexuality in a reptile". Nature. 332 (6167): 832–834. Bibcode:1988Natur.332..832G. doi:10.1038/332832a0. PMID   3357551. S2CID   4355596.
  9. ↑ Browne, Malcolm W. (10 May 1988). "In Lizards, Eggs' Heat Linked to Behavior". The New York Times. Retrieved 18 April 2016.
  10. ↑ Crews, David; Rushworth, David; Gonzalez-Lima, Francisco; Ogawa, Sonoko (2009). "Litter Environment Affects Behavior and Brain Metabolic Activity of Adult Knockout Mice". Frontiers in Behavioral Neuroscience. 3: 12. doi: 10.3389/neuro.08.012.2009 . PMC   2730751 . PMID   19707539.
  11. ↑ Crews, David; Gore, Andrea C.; Hsu, Timothy S.; Dangleben, Nygerma L.; Spinetta, Michael; Schallert, Timothy; Anway, Matthew D.; Skinner, Michael K. (2007). "Transgenerational epigenetic imprints on mate preference". PNAS. 104 (14): 5942–5946. Bibcode:2007PNAS..104.5942C. doi: 10.1073/pnas.0610410104 . PMC   1851596 . PMID   17389367.
  12. ↑ "Research Excellence Awards". The University of Texas at Austin. Archived from the original on 2016-06-30. Retrieved 2016-04-18.
  13. ↑ "Top 100 Science Stories of 2007". Discover Magazine. Discover. Retrieved 18 April 2016.
  14. ↑ Gillette, Ross; Miller-Crews, Isaac; Nilsson, Eric E.; Skinner, Michael K.; Gore, Andrea C.; Crews, David (2014). "Sexually Dimorphic Effects of Ancestral Exposure to Vinclozolin on Stress Reactivity in Rats". Endocrinology. 155 (10): 3853–3866. doi:10.1210/en.2014-1253. PMC   4164929 . PMID   25051444.
  15. ↑ Crews, David; Gillette, Ross; Miller-Crews, Isaac; Gore, Andrea C.; Skinner, Michael K. (2014). "Nature, Nurture and Epigenetics". Molecular and Cellular Endocrinology. 398 (1–2): 42–52. doi:10.1016/j.mce.2014.07.013. PMC   4300943 . PMID   25102229.
  16. ↑ Crews, David; Gillette, Ross; Scarpino, Samuel V.; Manikkam, Mohan; Savenkova, Marina I.; Skinner, Michael K. (2012). "Epigenetic transgenerational inheritance of altered stress responses". PNAS. 109 (23): 9143–9148. Bibcode:2012PNAS..109.9143C. doi: 10.1073/pnas.1118514109 . PMC   3384163 . PMID   22615374.
  17. ↑ Gillette, Ross; Miller-Crews, Isaac; Skinner, Michael K.; Crews, David (2015). "Distinct actions of ancestral vinclozolin and juvenile stress on neural gene expression in the male rat". Frontiers in Genetics. 6: 56. doi: 10.3389/fgene.2015.00056 . PMC   4345841 . PMID   25784924.
  18. ↑ Giudice, Linda (2012). "Epigenetic Transgenerational Inheritance of Altered Stress Responses". Proceedings of the National Academy of Sciences. F1000. 109 (23): 9143–9148. Bibcode:2012PNAS..109.9143C. doi: 10.1073/pnas.1118514109 . PMC   3384163 . PMID   22615374 . Retrieved 18 April 2016.
  19. ↑ Crews, David (2011). "Epigenetic Modifications of Brain and Behavior: Theory and Practice". Hormones and Behavior. 59 (3): 393–398. doi:10.1016/j.yhbeh.2010.07.001. PMC   3401366 . PMID   20633562.
  20. ↑ Crews, David; Gore, Andrea C. (2011). "Life Imprints: Living in a Contaminated World". Environmental Health Perspectives. 119 (9): 1208–1210. doi:10.1289/ehp.1103451. PMC   3230404 . PMID   21571618.
  21. ↑ Crews, David; Gore, Andrea C. (2012). "Epigenetic synthesis: a need for a new paradigm for evolution in a contaminated world". F1000 Biology Reports. 4: 18. doi: 10.3410/B4-18 . PMC   3434969 . PMID   22991583.
  22. 1 2 "Reptile Conservation International" . Retrieved 22 August 2023.
  23. ↑ "Undergraduate Biomedical Training Program The University of Texas at Austin". The Reproductive Biology Laboratory of David Crews. The University of Texas at Austin. Archived from the original on 9 October 2002. Retrieved 18 April 2016.
  24. ↑ "Contributor: David Crews". Huffpost. Retrieved 22 August 2023.
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