Psychabialagy 1988, Val. 16 (4), 321-334 The problem with gender

DAVID CREWS University of Texas at Austin, Austin, Texas

Websters defines gender as the classification of animate beings and inanimate things as mascu­ line, feminine, or neuter. When used as a concept that guides how we perceive and study sexual­ ity, gender becomes nebulous: To some, gender is defined in terms of behavior, whereas others regard gender as indicative of chromosome constitution. However, gender is an anthropocentric psychological construct that has little meaning when dealing with nonhuman organisms. In such investigations clarity and precision of definitions of sexuality are paramount. This essay demon­ strates that sexuality is not a unitary phenomenon, but rather a multifaceted composite of different sexes that may or may not be concordant. The essay further suggests that the components of sexuality be considered in terms of complementary mechanisms and outcomes.

The essential complementarity of sexual reproduction Gender Regarded as Behavior is expressed as dimorphisms, or consistent differences be­ Consider the commonly used categories of "male sex­ tween males and females in reproductive tissues and their ual behavior" and "female sexual behavior." There is functional products. These differences are often referred a basic problem with investigating the basis of these to as gender differences. As a concept in scientific gender-related behaviors, because (1) there are two sexes research, however, gender can be problematical. Because and (2) there is a tendency to define and describe each of the very nature of sexual reproduction, requiring as sex in relation to the other. Two sexes, then, becomes it does two sexes, gender has become a term used in differ­ a confounding variable in any experimental investigation ent ways to describe and account for many phenomena of gender-related behaviors. But is this inevitable? Such occurring at many levels of biological organization. For a question becomes important because if it were possible example, some define gender in terms of behavior, to "control" for the fact of two sexes, then it would be whereas others regard gender as indicative of chro­ possible to exarnine the extent to which sexual behaviors mosomal constitution. This vagary creates problems when are mutually exclusive or complementary. trying to determine the bases of sex differences. The mag­ nitude of this problem is not immediately apparent be­ Gender Regarded as Chromosomes cause, with the exception of pathology, these two elements In all mammals, the chromosomal constitution of go­ are fundamentally and functionally linked in the eutherian nadal males is different from that of gonadal females. But mammals and birds that are most often studied. Recent are sex chromosomes equivalent to, or even responsible research indicates that, when we look to the reptiles, the for, gender-related differences? Our concepts regarding ancestors of mammals and birds, some of our assump­ sexual differentiation have been based on organisms that tions about how sex chromosomes and sexual behaviors exhibit genotypic sex-deterrnining mechanisms. Were it are related are violated. The fact that in mammals and possible to obtain organisms that lack sex chromosomes birds males and females differ in both behavior and chro­ but that still exhibit sexual reproduction with its associated mosomes may seem to be an intractable confounding vari­ behaviors, we could begin to examine the genetic basis able in all sex differences research. This need not be true. of sexuality from a new perspective. This essay discusses two animal model systems in which EIsewhere, I have discussed the manifold meanings of behavior or chromosomes cannot be used to define gender . sex and the degree to which genetic sex, gonadal sex, ana­ In so doing, they give us a new perspective of the gener­ tornical sex, hormonal sex, and behavioral sex are as­ ality of some of our most fundamental assumptions regard­ sociated (Crews, 1987b). Here, I discuss two commonly ing gender-related traits. held perspectives of gender and how research with atypi­ cal animals allows one to circumvent the difficulties in­ herent in each. I show how study of a parthenogenetic whiptaillizard species that lacks males reinforces the con­ This paper is dedicated to the memory of Frank A. Beach. The research reported here was supported in part by Grant MH41770 and by Na­ clusions that (1) the categories of male sexual behavior tional Institutes of Mental Hea1th Research Scientist Award 00135 to and female sexual behavior leave an inaccurate picture the author. I wish to thank J. J. Bull, Martha McClintock, and Jane of sexuality; (2) the vertebrate brain contains dual neu­ Stewart for reading the manuscript. I have also benefited from J. J. Bull' s ral circuits, one that subserves mounting behavior and the drawing my attention to the elegance of Coyne's Rule, a recent clarifi­ other receptive behavior; and (3) the complementarity of cation of Haldane's Rule. Address correspondence to David Crews, In­ stitute of Reproductive Biology, Department of Zoology, University of specific behaviors is fundamental to successful reproduc­ Texas at Austin, Patterson Laboratories Building, Austin, TX 78712. tion. Study of the leopard gecko, a gonochoristic species

321 Copyright 1988 Psychonomic Society, Inc. 322 CREWS lacking a genotypic sex-determining mechanism, indicates Evolution of the Triploid Cnemidophorus uniporens that the genetic information relating to sexual behaviors need not be associated with sex chromosomes.

GENDER AS BEHAVIOR

Numerous studies indicate that most sexual behaviors differ between the sexes mainly in frequency. In gonochoristic species (separate sexes in separate in­ <;> c. inornofus x cf C. gu/oris dividuals), gonadal males are more likely to mount, whereas gonadal females are more likely to be mounted (hereafter called homotypical sexual behaviors). However, it is important to keep in mind that individuals can and normally do exhibit behaviors typical ofthe opposite sex (hereafter called heterotypical sexual behaviors). The dis­ play of heterotypical behaviors is common in many animals, particularly mammals (Beach, 1968; Dagg, 1984). For example, female-female mounting in cattle advertises estrus, whereas female-fema1e mounting in the rhesus monkey is important in maintaining social har­ mony. Thus, male sexual behavior and female sexual be­ havior more accurately refer to the probability that in­ dividuals possessing testes or ovaries will exhibit certain suites of displays and actions rather than astriet gonad­ <;> c. inornolus x cf F hybrid l*1 specificity ofthese behaviors. In those few instances that may be regarded as gonad-specific, such as the behaviors observed during ejaculation and nursing, the absence or abbreviated nature of the behavior in the opposite gonadal sex may be due to the diminished development or absence of the structures involved in the execution of the be­ havioral display (Kelley, 1988). The fact that individuals of each gonadal sex have the ability to behave as the opposite sex implies that neural substrates for both behaviors exist in each individual. How can we control for the presence of two sexes in sex differ­ Triploid C. uniparens ences research? Unisexual animals offer an unusual op­ Figure 1. Lineage of tbe a11-female wbiptaü Iizard, Cnemidopho­ portunity to study this problem since they are anatomi­ rus uniparens. See text for furtber details. cally and hormonally fema1e-like, yet retain behavioral bisexuality (Crews, in press). the matemal ancestral species has a certain trait-a poly­ The Wbiptail Lizards morphism in the behavioral sensitivity to progesterone­ The Cnemidophorus lizards of southem North America that may help explain why C. inomatus has been involved and Central and South America are a large and diverse in the production of at least nine parthenogenetic species. genus. Of the 45 species that constitute the genus, two­ Attempts to recreate the original hybridization event have thirds are gonochoristic, having both male and fema1e in­ not been successful. dividuals that reproduce sexually. However, fully one­ Only one cnemidophorine species (c. tigris) has been third of the species are unisexual, consisting only of in­ found to have heteromorphie sex chromosomes. As in dividuals that reproduce by true parthenogenesis. Most, mammals, the male is the heterogamete, but the degree if not all, of the parthenogenetic whiptail species are be­ of the chromosomal heteromorphism is reduced and con­ lieved to have a hybrid origin, and in many instances, the sidered to be at a primitive state of chromosomal evolu­ genealogy of the parthenogen is known. On the basis of tion (Bull, 1978; Cole, Lowe, & Wright, 1969). AlthoUgh cytogenetic evidence, Lowe and Wright (1966) proposed heteromorphie sex chromosomes are not evident in other that C. gularis is the patemal ancestor to the par­ sexual species, it is assumed that gonadal sex is deter­ thenogenetic whiptail, C. uniparens (Figure 1). More re­ mined by genetic mechanisms. Evidence for this hypothe­ cently, restriction endonuclease analyses of mitochondrial sis is that despite the lack of obvious sex chromosomes, DNA have established that C. inomatus is the matemal which also applies to species exhibiting environmental sex ancestor of C. uniparens (Densmore, Moritz, Wright, & determination (see below), the normal sex ratio of both Brown, in press). There is good reason to believe that the sexual and unisexual species are not altered when eggs THE PROBLEM WITH GENDER 323 are incubated under different temperatures (Crews & Bull, ing pseudosexual behaviors. Because males usually do not 1988). Finally, many, but not all, parthenogens are poly­ occur in unisexual organisms, the terms male-like and ploid (Dawley, in press). Jemale-like are used to refer to these pseudosexual be­ haviors. Sexual Versus Pseudosexual Behavior It is remarkable that both the sexual and the unisexual The fundamental difference between sexual and uni­ species of whiptaillizard exhibit a similar "mating" se­ sexual organisms makes it important to have subtle but quence (Figure 2). In the two parental gonochoristic spe­ necessary semantic roles. For example, although par­ eies, the male approaches and investigates the female with thenogenetic whiptails have ovaries and lack male genita­ his bifid tongue, presumably indicating involvement of lia, it is not appropriate to refer to them as females; "fe­ chemical senses via the vomeronasal organ. A sexually male" has meaning only in the context of "male." receptive female stands still for the male, allowing hirn However, parthenogenetic whiptails exhibit behaviors to mount her back. Usually just before the male mounts seen commonly in sexually active male whiptails during the female, he grips with his jaws either a portion of the mating. Since male-typical and female-typical sexual be­ skin on the female's neck or her foreleg. As the male rides haviors can refer only to those behavioral displays as­ the female, he scratches her sides and presses the female's sociated with males and females in gonochoristic species body against the substrate. The male then begins to (e.g., intrornission and receptive behaviors, respectively), maneuver his tail beneath the female's tail, attempting to it is not appropriate to use this terminology when describ- appose their cloacal regions. During mating, one of two

C. inornotus C uniporens C gu/oris

Figure 2. Sexual and pseudosexual behavior in whiptail Iizards. Mating sequence in the ancestral, sexually reproducing whiptail liz­ ards, Cnemidophoros inomatus Oeft panel) and C. gularis (right panel). Photos by P. DeVries. Middle panel: Pseudosexual behavior in the descendant, parthenogenetic whiptail lizard, C. uniparens. Photos by D. Crews. Note the similarity in the behavioral sequence to that 01 tbe gonochorlstic whiptail species. 324 CREWS hemipenes is everted through the male' s cloacal opening responsible for indueing male-like pseudocopulatory be­ and is intromitted into the female's cloaca. With intro­ havior (see below), the latency to ovulation is shortened mission, the male shifts his jaw-grip from the female's considerably (Crews et al., 1986). Tbis behavioral facili­ neck to her pelvic region, thereby assuming a contorted tation of ovarian growth also results in the production of copulatory posture, which I call the doughnut posture. many more eggs during the course of the breeding sea­ This posture is maintained for 5-10 min, after which the son. In nature, C. uniparens lay between 2 and 3 clutches male rapidly dismounts and leaves the female. per breeding season (Congden, Vitt, & Hadley, 1978; A virtually identical sequence of events has been ob­ Hulse, 1981). In captivity, isolated individuals lay viable served in at least five species of unisexual whiptail liz­ eggs, but the social environment has a pronounced effect ards (Crews & Fitzgerald, 1980) (see Figure 2). One in­ on fecundity. Isolated individuals lay an average of 0.8 dividual approaches and mounts another individual. After clutches, whereas individuals housed with conspecifics riding for a few minutes, the mounting (male-like) in­ displaying male-like pseudosexual behavior lay an aver­ dividual swings its tail beneath that of the mounted age of 2.5 clutches (Crews & Moore, in press; Gustaf­ (female-like) individual, apposing the cloacal regions. At son & Crews, 1981). Tbus, only those captive individuals the same time, the mounting individual shifts its jaw-grip able to engage in pseudosexual interactions exhibit nor­ from the neck to the pelvic region of the mounted in­ mal fecundity. Furthermore, housing intact individuals dividual, assuming the doughnut posture. Since the par­ together leads to a complementarity in their reproductive thenogens are morphologically female, there are no hemi­ conditions and an alternation in their roles in pseudosexual penes and intromission does not occur. Although this encounters. For example, if two intact individuals are phenomenon has been studied only in captivity, mount­ housed together, they quickly become 180 0 out ofphase ing behavior has been observed in the field (Grassman with one another in terms of both their ovarian activity & Lindzey, 1986). Similarly, pseudocopulatory behaviors and their behavior (Crews & Fitzgerald, 1980; Moore, have been reported in field studies of the parthenogenetic Whittier, Billy, & Crews, 1985). Behavioral facilitation morning gecko, Lepidodactylus lugubris (Brown, 1987; of reproduction also occurs in the parthenogenetic gecko, Crews, 1987c; Falanruw, 1972; Werner, 1980; Zawor­ L. lugubris (Brown & Sakai, in press; Falanruw, 1972). ski, 1987). The Reproductive Endocrinology of Sexual The Psychobiology of Sexual and and Unisexual Whiptail Lizards Pseudosexual Behavior In females of all vertebrates studied to date, the cir­ It is weIl established that in gonochoristic vertebrates, culating levels of estrogen increase as the follicle grows, the courtship and copulatory behavior of the male facili­ peaking around the time of ovulation (reviewed in Crews tates ovarian growth in conspecific females, in addition & Silver, 1985). Progesterone levels begin to increase to ensuring fertilization of female ova by male sperm. In­ during the latter stages of follicular maturation and reach deed, studies with representatives of all vertebrate classes their maximum following ovulation; progesterone con­ show that the sexual behavior of the male facilitates the centrations decline as the corpora lutea are resorbed. In environmental stimulation of ovarian recrudescence in the some species, the androgenic hormones are low through­ female (Crews & Silver, 1985). For example, in the musk out the ovarian cycle (as is the case in the whiptailliz­ shrew (Dryden, 1969), ring dove (Lehrman, 1965), green ards), whereas in others, androgens are elevated during anole lizard (Crews, 1975), rough-skinned newt (Moore, the follicular phase, the luteal phase, or in both. Simi­ 1987), goldfish (Stacey, 1987), and some coral reeffishes lady, in male vertebrates exhibiting an associated (Demski, 1987), the courtship behavior ofthe male syn­ reproductive pattern (Crews, 1984), concentrations of an­ chronizes and coordinates the reproductive physiology of drogens such as dihydrotestosterone and testosterone are the female. Often the female does not undergo normal highest during the breeding season while estrogen and ovarian development in the absence of sexually active progesterone secretions are low and monotonic (Crews males. In Cnemidophorus inornatus, the maternal ances­ & Silver, 1985). tor to C. uniparens, the courtship behavior of a sexually Tbe reproductive cycles of both female sexual whip­ active male is required for reproduction in the female tail lizards and the parthenogenetic whiptails consist of (Crews, Grassman, & Lindzey, 1986). Thus, this be­ aseries of discrete ovarian cycles, each approximately havioral facilitation of reproduction in gonochoristic ver­ 3-4 weeks in duration; both ovaries simultaneously ovu­ tebrates represents a potent selection pressure favoring late one to two eggs each (Moore, Whittier, & Crews, maintenance of male-typical behaviors. 1985). Following ovulation, corpora lutea form in the Pseudosexual behavior in the descendant unisexual spe­ ovary and the ova pass into the oviducts, where shell depo­ eies serves a function similar to that of male courtship sition occurs. Shelled eggs are usually laid 7-10 days af­ stimulation of female ovarian growth in gonochoristic spe­ ter ovulation. Production of a second clutch may be ini­ eies. Isolated parthenogens may eventually ovulate, but tiated within several days of oviposition. Experiments if other reproductively active individuals are present, more reveal further that the temporal patterns of ovarian hor­ will ovulate sooner (Crews et al., 1986). Furthermore, mone secretion are indistinguishable in the sexual and par­ if the cagemate is treated with progesterone, the hormone thenogenetic whiptaillizard species. THE PROBLEM WITH GENDER 325

and eopulatory behavior is dependent upon gonadal steroid hormones_Castrated males do not court females, but treat­ Behavlor ment of eastrates with exogenous androgens reinstates ~ ~ ~ eourtship and copulatory behavior (Lindzey & Crews, S,.uII S""II S .. u.1 1986). Signifieantly, about one-third of the castrates R.)actlon "Iupllvlly R"lclion respond with eomplete sexual behavior following adminis­ I. / .... ~~V~ Postovulatory tration of exogenous progesterone (Lindzey & Crews, 1988). It is important to note that progesterone-sensitive Laie ...;;; ~ males aetively eourt and eopulate with females with an GI CD c: Ovulation intensity equal to that shown by androgen-treated eas­ GI CI Mid trates. This suggests that C. inornatus is polymorphie in ~ S I ~ the eharaeter of a behavioral (i.e., brain) sensitivity to :; progesterone. Early ca ~ This finding of a polymorphism in the hormone­ Previtellogenlc .. behavior relationship in the sexual ancestral species is ex­ Prog.sleron. /-.. / eiting for two reasons_ First, it is eompletely opposite that found in studies on domestieated rodents and birds Hormones E.tro~ "\ (reviewed in Lindzey & Crews, 1986, in press). In these " ", ~ ~ ...... species, progesterone is an effective suppressor of sex­ And rogens-- -- ual behavior in males. That is, administration of ex­ Figure 3. Relation among sexual and aggressive behavior, circu­ ogenous progesterone to sexually aetive males reduces the lation concentration of sex steroid hormones, and ovarian state in frequeney and intensity of sexual behavior; when given the female whiptail Iizard, Cnemidophorus inornatus. in eonjunetion with androgen to castrated males, sexual behavior is not reinstated. The second reason this poly­ In the matemal aneestral species, C. inornatus, hor­ morphism in sensitivity to progesterone is of interest is monal fluetuations have predietable effects on sexual be­ that it rnay constitute an exaptation (Gould & Vrba, 1982), havior. In females, the receptive and aggressive behaviors or a feature that arose for one purpose but has been co­ vary with the stage of the ovarian eyde (Lindzey & opted during evolution to serve another purpose. Crews, 1988) (see Figure 3); sexual reeeptivity is ex­ The pseudosexual behavior of the parthenogen is also hibited only in the preovulatory stage, whereas previtel­ related to physiologieal state (Crews, 1987a) (see logenie and gravid females are highly aggressive. In Figure 4). Female-like behavior is limited to the pre­ males, eourtship and eopulatory behavior oceurs only ovulatory stage ofthe follieular eyde, whereas male-like when eireulating levels of testosterone and dihydrotestos­ behavior oceurs most frequently during the postovulatory terone are elevated, progesterone is low but unvarying, stages of the eyde. As might be expected, these behavioral and estrogen is undetectable (Moore & Crews, 1986). As roles during pseudocopulations are paralleled by differ­ is the ease with ferp.ale sexual receptivity, male eourtship ences in the eirculating levels of sex steroid hormones

BEHAVIOR

Female-like Male-like Female-like Male-like

OVARY

OVIDUCT

HORMONES

F"JgUre 4_ Relation lIIIlODg male-like and female-like pseudosexual bebavior, ovarian state, and circuIating concentrations of sex steroid bonnones during different stages of the reproductive cycle of parthenogenetic Cnemidophorus uniparens. 326 CREWS produeed by the ovary. Individuals show primarily mental stimulus to trigger male-like pseudosexual be­ female-like behavior during the preovulatory stage, when haviors. plasma estradiollevels are relatively high and progester­ The elose parallels in the nature and pattern of sex one levels relatively low. Male-like behavior is seen steroid hormone secretion in females of the sexual spe­ usually in the postovulatory phase, when estradiollevels eies and the parthenogens indicate that the evolution of are low and progesterone levels have inereased. parthenogenesis has not been accompanied by an altera­ The aneestral and deseendant speeies are alike in that tion of the usual pattern of endocrine changes. Although they are androgen-sensitive. Administration of exogenous the second alternative remains a possibility, recent experi­ androgens stimulates development of seeondary sex ments supporting the third alternative appear to exc1ude charaeters both early and late in development in both the second as a possibility. parthenogenetie and gonochoristic whiptail speeies It is a truism that behavioral transitions commonly oc­ (Crews, 1987a; Billy & Crews, 1986; Crews, Gustafson, cur at transitions in hormone concentrations in the blood. & Tokarz, 1983). For example, male-like pseudosexual There is an intriguingly elose parallel between the transi­ behavior ean be indueed readily in either intaet or ovariec­ tion from female-like to male-like pseudosexual behavior tomized parthenogens by hormone treatment. Refleeting and the three-fold decrease in circulating levels of estradiol their sexual aneestry, parthenogens respond to exogenous and the nine-fold rise in progesterone levels at ovulation testosterone or dihydrotestosterone treatment (Crews et (Figure 4). Is it possible that this shift in hormone con­ al., 1983; Crews & Moore, in press; Gustafson & Crews, centrations plays a crucial role in controlling expression 1981). However, radioimmunoassay of eireulating eon­ of pseudosexual behavior? Recent experiments suggest eentrations has uniformly failed to deteet plasma levels that the postovulatory surge in progesterone has been ex­ of these androgens at any stage of the reproduetive eyele ploited to serve as the trigger for male-like behavior in (Moore, Whittier, Billy, & Crews, 1985). Not only is the parthenogen. Recalling that ovariectomy abolishes all there no evidenee for transient surges in plasma andro­ pseudocopulatory behavior in parthenogens, I thought that gens during the course ofthe ovarian cyele, but individuals if progesterone were adminstered to one individual of a exhibiting male-like pseudosexual behavior are no more pair and estrogen to the other, pseudocopulations could likely to have detectable levels of testosterone or di­ be induced between two ovariectomized parthenogens. In­ hydrotestosterone than are lizards exhibiting female-like deed, pseudocopulations are seen only if one individual pseudosexual behavior. Thus, the parthenogens have re­ of such a pair is treated with progesterone and the other tained their sensitivity to androgens, but do not appear with an estradiol implant; furthermore, the progesterone­ to seerete deteetable amounts of androgens. implanted parthenogens always assume the male-like role Other observations support the conelusion that pseudo­ in the pseudocopulation (Grassman & Crews, 1986). It copulatory behaviors in uni sexual whiptails depend on is important to note here that other experiments with the steroid hormones, albeit not on androgens. First, pseudo­ sexual ancestral species have found that intact females copulatory behaviors have never been observed in housed in all-female groups mounted one another, with reproductively inactive individuals or in ovariectomized the male-like individual being postovulatory . Further­ individuals. Second, whereas female-like behavior is more, administration of progesterone to ovariectomized almost completely restricted to the yolk deposition phase, females has been found to stimulate female-female mount­ male-like behavior is most frequent in postovulatory , ing behavior (Lindzey & Crews, 1987). gravid animals. Third, the frequencies of male-like and Experiments in which each individual of a dyad was female-like pseudosexual behaviors exhibited by an in­ hormone treated (e.g., Grassman & Crews, 1986; Gustaf­ dividual change reliably during the course of the ovarian son & Crews, 1981) pointed to an important feature of cyele, with the result that two individuals alternate in both courtship and copulatory behavior. The principle of their physiology and their behavior. stimulus-response complementarity (Beach, 1976, 1979) There are several possible means by which steroid hor­ was originally modeled for sexually reproducing species. mones regulate pseudosexual behavior. First, the nature Briefly, the model suggests that a complementarity must and pattern of ovarian hormone secretion eould have been exist between the behavioral stimulus pattern (S) and the altered during the evolution of the parthenogen such that behavioral response pattern (R) if animals are to progress a sex steroid hormone proftle characteristic of males through the highly complex interactions required for resulted, thereby accounting for the expression of the reproduction. Because the principle of S-R complemen­ male-like pseudocopulatory behaviors. Second, progester­ tarity is independent of genetic and gonadal sex, female­ one, the precursor of all androgens, might be converted typical stimuli (in sexually reproducing species) tend to to androgens in their target tissues in the brain, exerting evoke male-typieal behavioral responses and male-typical its effect by serving as a prohormone. Third, the neural stimuli tend to evoke female-typical responses in both mechanisms subserving male-typical and female-typical gonadal males and gonadal females. For example, Beach sexual behaviors in the sexual ancestors could have been visualized this relationship as the mounting (S) of one in­ retained, but, in the absence of physiologicallevels of an­ dividual requiring the receptivity (R) of the other in­ drogen, co-opted another physiological and/or environ- dividual if mating was to occur. It is evident that this con- THE PROBLEM WITH GENDER 327 cept applies to asexual organisms as weIl. Although of minute amounts of the appropriate sex hormones originally restricted to organismal behavior, I believe this direct1y into these areas of gonadectomized individuals principle also has applicability to other levels of biologi­ restores mounting and receptive behaviors. cal organization where elements have co-evolved (e.g., The fact that the parthenogenetic whiptails exhibit male­ hormone-receptor relationships). like mounting and intrornission behaviors suggests that the neural circuits underlying these behaviors have been Brain Mechanisms Controlling Sexual and retained. This does not, however, provide the requisite Pseudosexual Behavior proof of the hypothesis that similar neural areas are em­ If the behaviors of the sexual ancestor and the par­ ployed in the display of pseudosexual behavior. Neuroen­ thenogenetic descendant are similar in form and in func­ docrine studies have determined that similar areas of the tion, are the neuroendocrine mechanisms underlying these brain are involved in the control of male-like pseudo­ behaviors also the same? It appears that the neural cir­ copulatory behavior in the parthenogens and in mount­ cuits utilized are similar, yet the hormonal cues that ini­ ing and intromission behavior in males of the sexual spe­ tiate sexual versus pseudosexual behavior are different. cies. This has been shown by two independent methods. There appear to be two distinct neural circuits that medi­ One approach in determining whether the brain areas ate sexual behaviors in vertebrates. Studies on represen­ involved in the display of male-like pseudosexual behavior tative species of all vertebrate classes agree in that por­ in the unisexual whiptails are the same as those areas con­ tions of the anterior hypothalamus and preoptic area trolling male-typical mounting and intromission behavior (AH-POA) are involved in the control of mounting and in the ancestral sexual species has been the intracranial intrornission behavior, whereas portions of the ventro­ implantation of steroid hormones. Results to date indi­ medial hypothalamus (VMH) are involved in sexual recep­ cate that androgen implanted into the AH-POA, but not tivity (Crews & Silver, 1985; Pfaff & Schwartz-Giblin, into the VMH, activates mounting behavior in both the 1988; Sachs & Meisel, 1988). The neurons residing in parthenogenetic descendant and sexual ancestral species these areas concentrate sex hormones, and implantation (Mayo & Crews, 1987; Rozendaal & Crews, in press)

P 0.16

Figure S. Schematic representation of the placement of hormone implants in the brain that elicited the doughnut copuJatory posture in whiptaillizards. Solid triangJes indicate androgen implants in studies with the parthenogenetic whiptaillizard, Cnemidophorus uniparens. Solid circles indicate androgen implants in studies with males of the gonochoristic ancestral species, C. inorruJtus. Open symbols represent place­ ment of implants that failed to elicit either male-Iike pseudocopulatory behavior in C. uniparens or male­ typical sexual behavior in C. inomatus. In aII experiments animaIs were gonadectomized at least 2 weeks prior to implantation. Numerals indicate distaoce posterior to zero point. LFB-Iateral forebrain bundle; POA-preoptic area; OC-optic chiasm; AC-anterior commlssure; ADVR-anterior dorsal ventricular rielge; AH -anterior hypotbalamus; OT -optic tract; VMH - ventromedial hypothalamus; OTE-optic tec­ tum; PC-posterior commissure; LIlA-lateral hypothalamic area. 328 CREWS

(see Figure 5); implantation of progesterone into the overlap might be the result of homology between the chro­ AH-POA, but not into the VMH, ofthe unisexual descen­ matin binding regions of the two receptors or the result dant elicits male-like behavior (Crews & Mayo, 1986). of similar acceptor regions within the genome. If, on the The mechanisms controlling receptive behavior involve other hand, progesterone proves to act through the an­ the VMH: when implanted into the VMH, but not into drogen receptor, this would suggest a fundamental differ­ the AH-POA, estrogen activates receptivity in C. uni­ ence in the mechanisms of hormone action at the genomic parens; estrogen has no effect on the display of male-like level in the whiptaillizards compared with allother ver­ behavior (Wade & Crews, 1988). tebrates studied to date. Another approach for investigating the brain mecha­ nisms controlling species-typical behavior is to study the GENDER AS CHROMOSOMES hormone-receptor interaction directly. Although experi­ ments indicate that the ancestral and descendant species Basic research on the mechanisms underlying sex de­ share similar neural circuits that control mounting be­ termination and sexual differentiation, mostly in domes­ haviors and, furthermore, that these neural circuits are ticated and inbred vertebrate species, has revealed that responsive to both androgen and progesterone, this is not upon fertilization, the genetic constitution of the individual evidence that the two hormones act via the same hormone is fixed. Thus, males and females differ at a fundamental receptors. genetic level. In mammals, the individuals we refer to as There are several possible explanations for the observed "males" have a dissimilar pair of chromosomes (XY), progesterone effects in whiptails. It is weIl established that whereas "females" have a sirnilar pair of chromosomes progesterone can rnirnic the actions of androgens by bind­ (XX); in birds, the opposite pertains, whereas in some ing to androgen receptors in the cell and translocating to reptiles, amphibians, and fish the heterogametic sex can the nucleus (Bardin, Brown, Isomaa, & Jänne, 1984). vary depending on the species (BuH, 1983). The deter­ Recall that the functional outcome of progesterone bind­ mination of genotype, in turn, results in the differentia­ ing to androgen receptors in mammals and birds is to in­ tion of the gonads, initiating a cascade of events that sculpt hibit sexual behavior in males. In progesterone-sensitive the differences between males and females. For exam­ male C. inornatus, however, progesterone stimulates sex­ pIe, the hormones secreted by the newly differentiated ual behavior. What is happening at the genomic level that ovaries and testes are critical to the differentiation of ac­ could account for these results? It is possible that the hor­ cessory sex structures and secondary sex characters, in­ monal specificity, but not the neural circuits thernselves, cluding the brain. Sexually dimorphic adult organisms that has changed. For example, it is possible that in the par­ must mate to contribute their genes to the next genera­ thenogenetic whiptail, progesterone activates male-like be­ tion are the end result. havior by binding to androgen receptors that were retained In a1l mammals and birds and in some reptiles, gonadal along with the neural circuits that control mounting be­ differentiation is a consequence of genotypic sex deter­ havior. This hypothesis is attractive, because the almost mination (aSO) mechanisms. In some reptiles, however, complete lack of circulating androgen in the parthenogen sex is determined by environmental sex determination would allow binding of even relatively weak agonists (ESO) mechanisms (BuH, 1983). The fundamental differ­ (e.g., progesterone) to androgen receptors. ence between aso and ESO mechanisms lies in the trig­ Another possibility is that progesterone acts by bind­ ger that initiates sex determination: in the former, gonadal ing to progesterone receptors that are functionally linked sex is determined at fertilization by the pairing of homolo­ to the neural circuits that control sexual behavior in males gous chromosomes, whereas in the latter, gonadal sex is of the ancestral species. This is supported by the finding determined later in embryogenesis as a consequence of that administration of R5020, a synthetic progestin, com­ the embryo's environment (Figure 6). They are alike, pletely restores homotypical sexual behavior in castrated, progesterone-sensitive males (Lindzey & Crews, in press). ENVIRONMENTAL SEX DETERMINATION Furthermore, administration of RU 486, an antiproges­ tin, to androgen-treated castrates fails to inhibit the resto­ ration of sexual behavior, yet prevents the induction of ~:~o ( 0.5 ------ZS.,...... -----) Environment sexual behavior in progesterone-sensitive males by progesterone (Lindzey & Crews, in press). This suggests that progesterone acts directly as a progestin in stimulat­ ing mounting behavior. Present efforts are focused on GENOTYPIC SEX DETERMINATION identifying and characterizing the progesterone and an­ drogen receptor systems in the brain. Sex ) If progesterone proves to act through its own receptors, Ratio 0.56,.,.------Environment this will suggest that the progesterone receptor and an­ drogen receptor overlap in their abilities to bind to and Figure 6. A schematic representation of the fundamental ditTer­ regulate specific regions on the genome responsible for ence hetween environmental sex determination and genotypic sex stimulation of specific behavior patterns. This functional determination. THE PROBLEM WITH GENDER 329

Determination of Gonadal Sex extent to which sexual dimorphisms are independent of genotype. In such species, there is no male or female ge­ nome established at fertilization; rather, the determina­ "0 tion of gonadal sex is triggered stricdy by an environmen­ c: tal stimulus. ~_ .5 o a. The Leopard Gecko o Q: The most thoroughly studied ESD system is temperature-dependent sex determination (BuH, 1980).

O-L--~~------~--- For example, in the leopard gecko (Eublepharis 32' macularius), gonadal sex is deterrnined by incubation tem­ Temperature perature, with relatively "hot" temperatures (32°C) resulting in 80% male offspring and 20% female off­ Figure 7. EtTect of temperature on primary sex ratio in the leopard spring, whereas relatively "cool" temperatures (26°C) gecko, Eublepharis macularius. result in only female offspring (Figure 7); the primary sex ratio is 50:50 at the intermediate temperature of29°C. however, in that in both, (1) the primary sex determiner It is important to note that intersexes are not produced operates solely as a trigger that initiates the events that (BuH, 1987; Wagner, 1980), and that even at the high in­ shape sex differences, (2) hormones secreted by the em­ cubation temperatures, the gonads of female individuals bryonie gonad govem the subsequent differentiation and are clearly ovaries (Figure 8). Histological examination development of other components of sexuality (Crews & of the ovaries of females from hot incubation conditions BuH, 1987; Wilson, George, & Griffen, 1981), and (hereafter hot females ) has not revealed any evidence of (3) intersexes or hermaphrodites are usuaHy not found. testieular fragments or ceHs. There are no evident differ­ Study has revealed that all ESD species appear to be ences between the ovaries of hot females and the ovaries gonochoristic, lack heteromorphie sex chromosomes, and of females from cold incubation conditions (hereafter cold have little if any genetic control over the determination females). of gonadal sex (BuH, 1983). Furthermore, BuH and coworkers have recendy found that the putative testis de­ The Effects of Incubation Temperature termining gene of mammals (Page et al., 1987) hybridizes on Adult Sexuality to DNA ofboth males and females in ESD reptiles (BuH, Incubation temperature of the embryo affects sexual Hillis, & O'Steen, 1988). Thus, species exhibiting ESD dimorphisms in the adult phenotype. Secondary sex present researchers with an opportunity to exarnine the characters in the leopard gecko include head dimensions,

Figure 8. Histology of gonads of adult leopard geckos that bad been incubated at 26°,29°, or 32° C. Top panel are ovaries, bottom panel are testes. Intersexes have never been observed. Photos by J. LaClaire. 330 CREWS

76 incubated at different temperatures. However, androgen levels are significantly higher and estrogen levels lower in hot females compared with cold females. 75 Based on the above information, one might predict that psychosexual differentiation in the sexes might also be 74 influenced by events in the eggs (Figure 10). Indeed, the sexual behavior of adult females varies according to the temperature they experienced in the egg.

73 • Female Sexual behavior in leopard geckos is stereotyped and o Male differs between the sexes. Tbe typical copulatory sequence 8 consists ofthe male's rapidly vibrating his tail on encoun­ ... 72 )C tering a female; females have never been observed to ex­ ~ hibit this behavior. It is assumed that tall wagging is Öl c: CI) elicited by the detection of a female-specific pheromone ..! 71 ~ (Mason & Gutzke, 1988). Males also rub the pubic area :§ (7) against the substrate, presumably depositing pheromone(s) 3: I in the exudate from the pubic pores. The male then ap­ ca~ 70 .., proaches the female and licks her tail. Tbe male next grips and shakes the female's tail; this biting and shaking is gen­ 69 tle and does not result in any discernible wounds. The male then shifts his jaw-grip to the female's back, neck, or head area, moving his body parallel to the female's 68 1(23) body. Again, this biting is very gentle. At this point, the female usually raises her tail and allows the male to ap­ 67 pose his cloacal region to hers, and intromission occurs. A receptive female remains stationary as a courting male first lieks and then grips her tail. As the male shifts his 66 grip to the female's back, neck, or head area, the female 26 29 32 raises her tail and allows intromission. A nonreceptive Temp (OC) female may terminate courtship at any point by either flee­ ing from the male, biting the male (generally causing tis­ Figure 9. Effect of incubation temperature on bead size in male and femaIe leopard geckos. Presented are tbe means and standard sue damage), throwing the male off her back, or display­ errors for adults of known incubation temperatures. Sampie sizes ing heterotypical (male-typical) behavior. sbown in parentbeses. Although all of the females tested to date have elicited comparable levels of courtship from male stimulus patent pubic pores, and cloacal swelling due to the hemi­ animals, indicating that males do not discriminate among penes. With the exception of cloacal swelling (females them, the responses of females to male courtship differ have never been observed to have hemipenes), these markedly depending upon the female's incubation tem­ meristic characters vary within each sex according to in­ perature (Gutzke & Crews, 1988) (see Figure 11). If she cubation temperature. Females from eggs incubated at is receptive, a cold female exhibits only sexual receptivity 32 0 C (hot females) have pronounced pubic glands with when courted by a male; no heterotypical behaviors are patent pores similar to those found in males; females from 0 0 eggs incubated at 26 C (cold females) and 29 C have Table 1 smaller glands and closed pores (Gutzke & Crews, 1988). Circulating CODCentrations of Total Androgens and Estradiol Head size also is sexually dimorphie in the leopard gecko. as Measured by Radioimmunoassay in Adult Leopard However, for a given sex, individuals from hot incuba­ Geckos (Eublepharis macularius) tion temperatures bad significantly wider heads than those Total Estradiol from cold incubation temperatures (Figure 9). Incubation Androgens Tbe endocrine physiology of the adult is also influenced Temperature Number M SD M SD by the temperature experienced during incubation. Radio­ Female immunoassay of circulating concentrations of sex steroid 26°C 4 0.36 0.07 0.88 0.13 hormones reveals systematic differences in the levels of 29°C 7 1.23 0.45 0.49 0.05 0.41 0.10 total androgens and estradiol both between and within the 32°C 5 6.06 2.11 sexes (Gutzke & Crews, 1988) (see Table 1). Overall, Male circulating concentrations of total androgens in adult fe­ 29°C 6 77.92 26.40 0.48 0.06 males are lower than in adult males; levels of estrogen 32°C 9 31.67 4.33 0.37 0.04 do not differ between the sexes. No significant differences Note-Mean concentration in ng/ml is presented witb ± I standard er- are detected in the hormonal proflles of males from eggs ror (see Gutzke & Crews, 1988). THE PROBLEM WITH GENDER 331

Determination of Behavioral Sex observed. Hot females, however, respond frequently with heterotypical behaviors; that is, these females respond to male courtship as ifthey themselves are males. This sug­ gests that it is the female's perception of self, and not her

Q) appearance to others or her willingness to mate, that has c: '"o been influenced by incubation temperature. It is interest­ '4 ing to note that over a 2-year period, no hot female has Q) a:'" been observed to mate or lay eggs. Hot females appear o~ to be functionally sterile, but the level at which the steril­ > ity occurs (gonad and/or brain) remains to be determined. ~ '"Q) al In mammals, administration of androgen to neonatal fe­ males results in a functional sterilization due to a mas­ culinization of the neural circuits subserving ovulation Temperature (Goy & McEwen, 1980; Yahr, 1988). It is possible that in adult geckos, the temperature during incubation deter­ Figure 10. Hypothetical model of adult psychosexual sexual mines the sex steroid hormones produced during gonadal differentiation of gonadal female leopard geckos incuhated at differ­ differentiation, and results in the observed differences in ent temperatures. See text for further details. reproductive behavior.

A HOMOTYPICAL BEHAVIOR MALE FEMALE

MOUNTING ALLOWS MOUNTING

(10) ...;d~ __.... .'.8) BACK GRIP g. TAIL ARCH TAIL GRAB (12) -----.-----.. ALLOWS TAIL GRAB (11) (6)

TAIL lICK ALLOWS TAIL LlCK

TAIL WAG REMAINS STATIONARY a: o ~ NO RESPONSE NO RESPONSE ::r: w co ..J I- MOUNTING ALLOWS MOUNllNG ~/,).. w ~ BACK GRIP lAlL ARCH

TAIL GRAB ALLOWS lAlL GRAB

lAlL LlCK ALLOWS lAlL LlCK

lAlL WAG REMAINS SlATIONARY

NO RESPONSE NO RESPONSE

INCUBATION TEMPERATURE (C)

Figure 11. Effect of incubation temperature on psychosexual differentiation in the leopard gecko. Presented are the average median behavioral responses of adult leopard geckos in tests with both male and female stimulus animals. (A) Homotypical response refers to sexual behaviors typical of individuals of the same gonadal sex. (B) Heterotypical response refers to sexual be­ haviors characteristic or individuals of the opposite gonadal sex. Sampie sizes are in parentheses. 332 CREWS

There were no differences in the frequencies of homo­ ciple of complementarity exists at an organismallevel as typical or heterotypical behavior in males from different weIl. It is only when such complementarity exists at all incubation temperatures in response to both male and fe­ levels that mating and reproduction are successful. male stimulus animals (Gutzke & Crews, 1988) (see The second animal model system, the leopard gecko, Figure 11). Males are produced over a smaller range of is one in which individuals lack a genotypic sex­ temperatures than are females (3 0 versus 6 0 C) (see determining mechanism. Attempts to alter the primary sex Figure 7), and this may be why less behavioral variation ratio in marnmals and birds have been singularly unsuc­ is observed. cessful (Charnov, 1982; Kiddy & Hafs, 1971), the few Agonistic behavior in both sexes also is affected by in­ exceptional cases of naturally occurring sex ratio biases cubation temperatures. Both males and females are more notwithstanding (Hrdy, 1988). The discovery that tem­ likely to exhibit aggressive behavior if they experienced perature, an easily regulated stimulus, deterrnines gonadal high temperatures during incubation; this relation is found sex in some reptiles presents a totally new avenue of ap­ whether animals were tested in their horne cage or in proach for investigators of sexual differentiation and a neutral site (Gutzke & Crews, 1988). Incubation tem­ gender-related behaviors. Temperature, the primary de­ perature also affects the probability of aggressive be­ terminer of gonadal sex in this species, also affects differ­ havior by males toward other males, but not toward fe­ ent levels of sexuality. The recent demonstration that the males. However, hot females are equally aggressive morphology, physiology, and psychosexual behavior of toward either sex. adults of both sexes is influenced by the temperature ex­ perienced as an embryo indicates that these effects are CONCLUSIONS permanent and profound.

I have discussed two animal model systems that give ENVOI new perspectives on fundamental problems in sex­ differences research. The first animal model system, the An evolutionary perspective reveals that at least some parthenogenetic whiptaillizards, illustrates a way of ex­ of the assumptions in present-day theories of vertebrate arnining the neural and endocrine correlates of sexual be­ sexual differentiation, based on studies of a restricted haviors that are not possible in mammals. The par­ number of eutherian marnmals, may be overlY narrow. thenogenetic whiptail lizard does not need a male to For example, the classical view is that all sornatic sexual reproduce, yet it continues to exhibit both male-like and dimorphisms, including brain, and hence behavior, result female-like pseudosexual behaviors. The fact that the neu­ from gonadal hormone production that begins after mor­ ral substrates of pseudocopulatory behavior did not phological differentiation of the gonad. Specifically, it is originate in unisexual whiptails, but were retained from weIl established from research on eutherian mammals that their sexual ancestors, reflects in part the organization of it is only after gonadal differentiation that the Leydig ceIls the vertebrate brain, with its dual neural substrates for secrete androgen that stimulates the development of the mounting and receptive behaviors. male reproductive tract; the Sertoli ceIls secrete Mullerian This animal model system also suggests how neuro­ Inhibitory Substance, which inhibits the development of endocrine mechanisms that control complex behaviors the female reproductive tract (George & Wilson, 1986; may evolve. The parthenogenetic whiptails do not secrete Wilson et al., 1981). detectable concentrations of androgen, so some other cue I have discussed how gender is neither behavior nor must trigger the male-like pseudocopulatory behavior. chromosomes. There also is good reason to suggest that This hormonal cue is probably the postovulatory surge gender is not gonads or hormones. In the tammar wal­ of progesterone. In the ancestral sexual species, court­ laby (Macropus eugenii), a metatherian marnmal, sexual ship and copulatory behavior in males is dependent upon differentiation of somatic structures begins weIl before testicular androgens, yet some males are behaviorally sen­ gonad determination (Wai-Sum, Short, Renfree, & Shaw, sitive to progesterone. This feature of the brain of the an­ 1988). Furthermore, there is evidence that sexual dimor­ cestral species, in this instance a sensitivity to progester­ phisms in such species are not dependent on sex steroid one of the neuroendocrine mechanisms subserving hormones; administration of exogenous androgens or mounting and intromission behavior, has been co-opted estrogens to pouch young fails to stimulate or inhibit in the descendant species in the form of a novel development of secondary sex characters (Fadem & hormone-brain behavior relationship. That is, this poly­ Tesoriero, 1986; Renfree, Short, & Shaw, 1987). It is morphism in progesterone sensitivity may have been the of particular interest to see increasing evidence that even substrate on which selection acted. in eutherian mammals there are apparent sex differences Finally, research on the unisexual lizards illustrates that precede gonadal differentiation: extragonadal effects nicely the complementarity at both the behavioral and of sex chromosomes (Scott & Holsen, 1977), altered sex physiologicallevels (Beach, 1976, 1979). The apparently ratios of live young after transfer of fast and slow develop­ universal requirement that females must be stimulated by ing mouse embryos (SeIlar & Perkins-Cole, 1987; the behaviors typical of males of their species to show Tsunoda, Tokunaga, & Sugie, 1985), and parental in­ normal ovarian growth (and vice versa) indicates this prin- heritance of methylation patterns (Swain, Stewart, & THE PROBLEM WlTH GENDER 333

Leder, 1987). Taken together, these results suggest that CREWS, D. (in press). Unisexual organisms as model systems for research even in eutherian mammals, there may be genes that are in the behavioral neurosciences.ln R. Dawley (Ed.), Biologyofunisex­ primarily responsible for the differentiation of secondary ual organisms. Ithaca, NY: Allen Press. CREWS, D., & Buu., J. J. (1987). Evolutionary insights from reptilian sex characters, perhaps even in the brain. Further study sexual differentiation. In F. P. Haseltine, M. E. McClure, & E. H. of "experiments ofnature" such as those described here, Goldberg (Eds.), Genetic markers of sex differentiation (pp. 11-26). or study of other as yet unutilized species such as simul­ New Y ork: Plenum. taneous and sequential hermaphrodites, will be important CREWS, D., & BULL, J. J. (1988). No apparent temperature-dependent to developing more general theories of gender differences sex detennination in congeneric sexual und parthenogenetic lizards. Manuscript submitted for publication. in vertebrates. CREWS, D., & FITZGERALD, K. (1980). "Sexual" behavior in par­ thenogenetic lizards (Cnemidophorus). Proceedings ofthe National Academy of Science U.S.A., 77, 499-502. REFERENCES CREWS, D., GRASSMAN, M., & LINDZEY, J. L. (1986). Behavioral facili­ tation of reproduction in sexual and unisexual whiptaillizards. Proceed­ BARDIN, C. W., BROWN, T., IsoMAA, V. V., &JÄNNE, O. A. (1984). illgs of the National Academy of Sciellce U.S.A., 83, 9547-9550. Progestins can mimic, inhibit, and potentiate the actions of andro­ CREWS, D., GUSTAFSON, J. E., & TOKARZ, R. R. (1983). Psychobiology gens. Pharmaceutical Therapeutics, 23, 443-459. ofpartbenogenesis in reptiles. In R. B. Huey, E. R. Pianka, & T. W. BEACH, F. A. (1968). Factors involved in the control of mounting be­ Schoener (Eds.), lizard ecology (pp. 205-231). Carnbridge, MA: Har­ havior by female mammals. In M. 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