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Draft:Female masculinization hypothesis

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Spotted Hyena (Crocuta crocuta) female, the original species in which the Female Masculinization Hypothesis was studied and proposed.

The female masculinization hypothesis suggests that exposure to androgens during prenatal development can result in masculinized behavioral, morphological, or physiological traits in female mammals. This hypothesis was first proposed in the context of research on spotted hyenas (Crocuta crocuta), where females exhibit male-like characteristics, including a pseudopenis and elevated aggression. Early work by Laurence Glickman and colleagues in the 1980s and 1990s documented how high levels of prenatal androgens influenced the development of these traits in hyenas, providing a foundation for the hypothesis.

Subsequent studies expanded the hypothesis to other species, such as meerkats (Suricata suricatta) and banded mongooses (Mungos mungo), where dominant females often display increased aggression and other masculinized traits linked to reproductive competition. The female masculinization hypothesis continues to be a focal point for exploring the intersection of endocrine mechanisms, sexual selection, and evolutionary ecology.

Historical Background

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The female masculinization hypothesis emerged from decades of research on mammalian development, social behavior, and endocrinology, with its origins deeply rooted in studies of the spotted hyena (Crocuta crocuta). Early naturalists and behavioral ecologists were struck by the unusual characteristics of female spotted hyenas, particularly their male-like dominance, aggressive behavior, and the presence of a pseudopenis—an enlarged, erectile clitoris that closely resembles the male penis. These traits challenged traditional understandings of sexual dimorphism and raised questions about the developmental processes underlying them.[1]

Initial studies in the mid-20th century documented the peculiar social and reproductive traits of spotted hyenas. Hans Kruuk’s seminal fieldwork in the 1970s provided detailed accounts of their matriarchal social structure, where females dominated males in both size and behavior. However, the physiological mechanisms driving these traits remained poorly understood until advances in endocrinology provided new tools for investigation.[2][3]

Laurence Glickman and his team at the University of California, Berkeley, were among the first to systematically investigate the role of prenatal androgens in the development of masculinized traits in female spotted hyenas. Their groundbreaking research in the 1980s and 1990s demonstrated that high levels of androgens produced by the mother during pregnancy were linked to the development of both the pseudopenis and aggressive behaviors in female offspring.[4][5][6]

A female meerkat, a species with dominant females in cooperative breeding systems. Females exhibit elevated aggression and androgen-linked traits.

Key studies by Glickman as of 1992 revealed that androgen exposure in utero was critical for the formation of masculinized genitalia, while additional research explored the organizational effects of these hormones on behavior. For example, their experiments showed that manipulating androgen levels during gestation could alter the degree of masculinization in both morphology and social interactions. This work provided the foundation for the formal articulation of the female masculinization hypothesis.[7][8]

Following its development in the context of spotted hyenas, the hypothesis was expanded to explain similar traits observed in other mammals. Research by Tim Clutton-Brock and colleagues on meerkats (Suricata suricatta) highlighted how dominant females in cooperative breeding systems exhibited elevated aggression and androgen-linked traits, such as increased body size and reproductive control. Parallel studies on banded mongooses (Mungos mungo) and other species demonstrated that masculinized traits in females often correlated with intense intra-sexual competition or high social dominance, suggesting a broader applicability of the hypothesis.[9][10][11]

The female masculinization hypothesis gained traction as it aligned with emerging frameworks in behavioral endocrinology, particularly the organizational-activational hypothesis. This model, which describes how hormones shape behavior and physiology during critical developmental windows, provided a theoretical backbone for understanding the lasting effects of prenatal androgen exposure. Advances in molecular techniques, such as hormone assays and gene expression analyses, further validated and refined the hypothesis.[12][13][14]

Despite its influence, the hypothesis faced early critiques. Some researchers questioned whether environmental factors, such as social stress or ecological pressures, could explain the observed traits without invoking prenatal androgen exposure. Others debated whether masculinized traits always conferred adaptive advantages or represented evolutionary trade-offs. Subsequent studies addressing these critiques refined the hypothesis, emphasizing the complex interplay of genetic, hormonal, and environmental influences on development.[15][16][17]

Over time, the female masculinization hypothesis has become a cornerstone for understanding the evolution of sexual dimorphism and the adaptive roles of hormonal mechanisms in shaping mammalian behavior. Influential reviews and interdisciplinary collaborations, including work by Kay Holekamp, Christine Drea, and others, have extended its relevance to broader questions in evolutionary ecology and conservation biology.[18][19]

Mechanisms

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The female masculinization hypothesis is rooted in the effects of prenatal androgens—hormones like testosterone—that influence the development of male-associated traits in females. These mechanisms involve hormonal, genetic, and epigenetic factors, shaping both morphology and behavior through distinct developmental processes.

Role of Prenatal Androgens

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Prenatal androgens play a central role in the masculinization of tissues and behaviors. During critical periods of fetal development, elevated androgen levels influence the differentiation of reproductive organs, neural structures, and behavioral tendencies. For example, in spotted hyenas (Crocuta crocuta), high androgen concentrations in pregnant females contribute to the formation of a pseudopenis and male-like social dominance in female offspring.[7][8][12]

The effects of androgens are commonly categorized as:

  • Organizational Effects: Permanent changes established during early development, such as the masculinization of genitalia and brain structures.
  • Activational Effects: Temporary changes triggered later in life, often during puberty, that amplify pre-established traits, such as aggression and dominance behaviors.[20][21]

Morphological Masculinization

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Prenatal androgen exposure can result in the development of male-typical anatomical features in females:

  • In spotted hyenas, the fusion of the labia and elongation of the clitoris to form a pseudopenis are direct consequences of androgenic effects on the urogenital sinus.[7]
  • Similar masculinized genital traits have been documented in other mammals, such as certain rodent and carnivore species, though the extent and visibility of these traits vary across taxa.[22]

Behavioral Masculinization

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Masculinized behaviors, including increased aggression, dominance, and territoriality, are also linked to prenatal androgen exposure. Neural pathways that regulate these behaviors are shaped by androgenic effects during development:

  • In meerkats, dominant females with elevated androgen levels exhibit aggressive behaviors typically associated with males, aiding in maintaining their social hierarchy.[23]
  • Similar effects have been observed in banded mongooses and other cooperative breeders where reproductive competition is intense.[24]

Genetic and Epigenetic Influences

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  • Genetic Pathways: Androgen receptors mediate the effects of hormones on target tissues. Variations in receptor density and sensitivity influence how masculinized traits manifest.[25]
  • Epigenetic Modifications: Environmental and maternal conditions can modulate the hormonal milieu during development, influencing gene expression and shaping phenotypic outcomes.[26]

Comparative Insights

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Although the specific effects of androgens vary across species, the underlying principles of prenatal hormonal influence remain consistent. Differences in the timing, intensity, and duration of androgen exposure account for the diversity of masculinized traits observed among mammals.

Evidence Across Species

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The female masculinization hypothesis suggests that under certain conditions, female mammals may exhibit masculine traits in behavior, morphology, and physiology, often due to increased exposure to androgens, particularly testosterone, during critical periods of development. This hypothesis has been explored across various species, providing evidence for how such masculinization can manifest in different ways.[27]

A Norway rat. Females with higher prenatal testosterone may show reduced maternal care and increased territoriality.

Rodents

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In rodent species, particularly laboratory mice and rats, androgen exposure during prenatal and postnatal development has been shown to alter sexual differentiation. Females exposed to elevated levels of testosterone during gestation or immediately after birth often display masculinized behaviors, including increased aggression, exploration, and mounting behavior typically associated with males. These behaviors are commonly studied in rodent models that have been manipulated genetically or hormonally to study sex differences. For instance, studies on house mice (Mus musculus) and Norway rats (Rattus norvegicus) have demonstrated that females with higher prenatal testosterone levels may show reduced maternal care and increased territoriality, behaviors typically more common in males.[28][29][30][31][32][33]

A female rhesus macaque. Females with higher levels of testosterone during the prenatal period exhibit more dominant behaviors (higher social ranking and increased aggression).

Primates

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In primates, particularly non-human primates such as rhesus macaques (Macaca mulatta) and vervet monkeys (Chlorocebus pygerythrus), evidence for the female masculinization hypothesis comes from observations of behaviors and morphological traits that resemble male counterparts in females with elevated androgen exposure. For example, female rhesus macaques with higher levels of testosterone during the prenatal period exhibit more dominant behaviors, such as higher social ranking and increased aggression compared to their female counterparts with normal testosterone levels. Furthermore, in some primate species, females may develop more male-like physical traits, including increased size or altered secondary sexual characteristics, which can be linked to hormonal imbalances during development.[34][35][36][37][38]

A ewe (female sheep). Exposure of high levels of testosterone during fetal development can lead ewes to mount other females and display other male-associated traits.

Ungulates

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Among ungulate species such as sheep and cattle, female masculinization has also been observed under the influence of hormones. Female sheep (Ovis aries) that were exposed to high levels of testosterone during fetal development often exhibit masculine behaviors, including mounting other ewes and engaging in male-like sexual behaviors. This phenomenon is thought to be due to maternal stress or hormonal fluctuations that alter the hormonal environment of the developing fetus. Similarly, in cattle (Bos taurus), females with abnormal androgen levels often show signs of masculinization in terms of both behavior and morphology, such as increased body size and altered reproductive anatomy.[39][40][41][42][43]

A female wolf. In many canine species such as this, elevated exposure to androgens can increase aggression and territorial marking in females.

Carnivores

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In carnivorous mammals, such as domestic dogs (Canis lupus familiaris) and wild species like wolves (Canis lupus), female masculinization has been documented in certain breeds or populations that exhibit elevated androgen exposure, which can result in increased male-typical behaviors such as territorial marking and aggression. Studies in these species have shown that such masculinization is not solely a result of genetic differences but can also be influenced by environmental factors, such as exposure to endocrine-disrupting chemicals.[44][45][27]

A Little brown bat. In populations with high levels of androgen exposure, females may show male-typical vocalizations and behaviours.

Bats

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Some studies on bats, particularly in species like the little brown bat (Myotis lucifugus), have also contributed to the understanding of female masculinization. In certain populations, females exposed to high androgen levels exhibit male-like vocalizations and mating behaviors. These behaviors can influence their social roles within the group and, in some cases, may lead to alterations in reproductive success, as masculinized females may compete more aggressively for mates or territories.[46][47]

Livestock and Domesticated Animals

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In domesticated species, female masculinization has been studied extensively due to its implications for animal husbandry and breeding. In particular, female pigs (Sus scrofa domesticus) and horses (Equus ferus caballus) have been subjects of study in which exposure to androgens has been linked to increased male-typical behaviors. In some cases, masculinized females are more aggressive, less likely to display maternal behaviors, and show altered reproductive cycles. This has led to investigations into how androgen manipulation during development might be used to improve productivity or manage behavior in domestic species.[48][49][50]

The evidence across various mammalian species supports the female masculinization hypothesis, demonstrating that androgen exposure during critical developmental windows can lead to the expression of male-typical traits. These findings have implications for understanding sexual differentiation, reproductive behavior, and social roles in mammals, as well as for applied fields like animal breeding and conservation.

Evolutionary Implications

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The female masculinization hypothesis has significant evolutionary implications, shedding light on the role of hormones in shaping sexual dimorphism, reproductive strategies, and social dynamics across species. Understanding how and why females may develop male-typical traits under certain conditions provides valuable insights into evolutionary pressures, mechanisms of sexual selection, and the flexibility of sexual differentiation processes in mammals.

Sexual Selection and Reproductive Strategies

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One of the key evolutionary implications of female masculinization is its potential impact on sexual selection. In species where masculinized females exhibit behaviors or physical traits typically associated with males, such as increased aggression, territoriality, or dominance, there may be changes in mating dynamics. In some cases, females with masculine traits could gain an advantage in securing mates or competing for resources. For example, in species where males typically compete for dominance, masculinized females may have the opportunity to access mates more effectively or even engage in mate guarding. This shift can alter traditional mating hierarchies and reproductive strategies, especially in species where female choice plays a critical role in mate selection.[51][52][53]

In some species, feminized males—males with characteristics typically associated with females, such as nurturing behaviors or higher parental investment—have also been observed, creating a broader context for understanding sexual selection. This duality between masculinized females and feminized males could reflect adaptive strategies that optimize reproductive success under varying environmental conditions.[54][55][56]

Sexual Dimorphism and Evolutionary Flexibility

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The female masculinization hypothesis also underscores the evolutionary flexibility in sexual dimorphism, the condition where males and females of a species exhibit distinct physical or behavioral differences. While sexual dimorphism is common in many species, it is typically seen as the result of selective pressures on males to exhibit traits that increase their chances of reproduction, such as larger size, stronger features, or more elaborate courtship displays. However, female masculinization challenges the rigid distinction between male and female traits, suggesting that under certain conditions—such as hormonal imbalances or environmental stress—females can also exhibit male-typical traits.[57][58][59]

This flexibility could have evolutionary advantages, allowing populations to adapt to fluctuating environmental pressures. For example, in species with skewed sex ratios or where males are scarce, females with masculinized traits may be able to fill reproductive niches traditionally occupied by males, ensuring the survival and continuation of the population. In such cases, the development of masculine traits in females could be a form of sexual plasticity, helping species navigate changing ecological conditions.[60][61][62]

Hormonal Influences on Evolutionary Development

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Hormonal influences on sexual differentiation are not only central to the development of individual organisms but also have broader evolutionary implications. The female masculinization hypothesis suggests that variations in androgen exposure during critical developmental periods can lead to lasting effects on behavior and physiology, potentially influencing natural selection over time. For example, if masculinized females exhibit enhanced survival traits—such as increased aggression that helps protect offspring or territory—these traits may be favored by natural selection, even in females. This highlights the potential for hormones to drive evolutionary change in ways that go beyond the typical male-female distinctions.[63][64]

In species with environmental stressors, such as pollution or changes in habitat, exposure to endocrine-disrupting chemicals can mimic the effects of increased androgen levels, leading to unexpected shifts in sexual behavior and traits. Such changes could have long-term evolutionary consequences, possibly influencing how species adapt to changing environments or how they respond to anthropogenic pressures.[65][66][67]

Impact on Social Structure and Evolutionary Roles

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The expression of male-typical traits in females can also affect social structures and roles within species. In social mammals, particularly those with complex social hierarchies (such as primates, wolves, or elephants), masculinized females may challenge traditional gender roles, leading to shifts in leadership, dominance, and cooperative behaviors. In some cases, these females may form alternative mating strategies or leadership structures, which could alter the overall dynamics of group living.[68][69][70]

The evolutionary impact of such shifts is particularly relevant in species where cooperation between males and females is key to survival. If masculinized females are able to contribute to or even dominate certain aspects of the social structure (such as by engaging in male-typical behaviors like aggression or territory defense), this could drive changes in the evolution of cooperation, leadership, and resource distribution within groups.[71][72][73]

Evolution of Parental Investment

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The evolution of parental investment is another critical area affected by female masculinization. In species where males typically invest heavily in parental care, the appearance of masculinized females who take on more active roles in offspring care or territorial defense could alter the reproductive strategies of both sexes. For example, in certain rodent species, masculinized females may be more aggressive in defending nests or resources, potentially improving offspring survival. This shift in parental roles may influence the evolution of parenting behaviors across generations, reshaping the traditional division of labor between sexes.[74][75][76][77]

Critiques and Controversies

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While the female masculinization hypothesis has garnered significant interest in the fields of endocrinology, evolutionary biology, and animal behavior, it is not without its critiques and controversies. These center around concerns regarding the generalizability of findings, the complexity of hormonal interactions, and the ethical implications of research in this area.

Over-Simplification of Hormonal Influence

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One major critique of the female masculinization hypothesis is the potential over-simplification of the relationship between hormonal exposure and the development of masculine traits. While androgens like testosterone play a central role in sexual differentiation, critics argue that the hormonal environment is complex and influenced by a multitude of factors. These include genetic variation, environmental influences, and interactions between different hormones, which can complicate the interpretation of findings. In some cases, elevated androgen levels may not consistently lead to masculinized behaviors or characteristics, and individuals may exhibit a range of responses depending on their genetic and developmental context. Thus, attributing masculine traits solely to hormonal imbalances may not fully capture the complexity of sexual differentiation.[78][79][80][81]

Interpreting Behavioral Changes

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The interpretation of behavioral changes in masculinized females is also a point of contention. Critics argue that behaviors associated with masculinization, such as aggression, increased territoriality, or dominance, may be more nuanced than simply being male-typical traits. For instance, many behaviors attributed to masculinization may reflect adaptive responses to environmental pressures, social structures, or reproductive strategies rather than a direct expression of male-like traits. This raises questions about whether behaviors like aggression or dominance truly represent a form of masculinization or whether they are part of broader strategies to cope with ecological or social challenges. As such, some researchers caution against over-interpreting behavioral differences as a clear sign of masculinization without considering the full ecological and social context.[82][83][84]

Bias in Research Models

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Another area of concern is the potential bias in the research models used to study female masculinization. Much of the research in this area has been conducted in species with well-established laboratory populations or domesticated animals, which may not accurately represent natural variation in wild populations. These species may be subject to artificial selection pressures or other human interventions that could influence the expression of masculinized traits. In addition, the focus on a small number of model species may limit the generalizability of findings to other mammals, especially those with different ecological niches, social structures, or reproductive strategies.[85][86][87][88]

Ethical Concerns and Manipulation of Hormones

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The manipulation of hormones in animal models to study female masculinization also raises ethical concerns, particularly when it comes to animal welfare. Hormonal interventions, such as administering synthetic androgens or altering prenatal hormone exposure, can have unintended consequences on the health and well-being of the animals involved. For example, exposing female animals to elevated testosterone may result in physical deformities, altered reproductive function, or behavioral changes that are not typical for their species. These concerns highlight the need for careful consideration of the ethical implications of such studies, especially in terms of balancing scientific advancement with the responsibility to minimize harm to research subjects.[89][90][91]

Questioning the Universality of Female Masculinization

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Some researchers have raised questions about whether the concept of female masculinization is universally applicable across species. While the hypothesis has been supported in several mammalian species, there are notable exceptions where females do not exhibit significant masculinized traits, even when exposed to elevated androgen levels. Additionally, in species with highly rigid sex roles or clear-cut sexual dimorphism, the potential for female masculinization may be limited or absent altogether. This has led some to argue that the hypothesis may not be as broadly relevant as initially thought and that its application may be constrained by factors such as evolutionary history, ecological context, and species-specific reproductive strategies.[92][93][94]

Potential for Misinterpretation

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The concept of female masculinization has also faced criticism for being potentially misinterpreted in a socio-cultural context. Some critics argue that framing female behaviors or traits as "masculine" could reinforce gender stereotypes and perpetuate harmful biases about what is considered "appropriate" behavior for women, both in humans and in animals. These concerns highlight the importance of using careful and neutral language when discussing masculinization in the animal kingdom, as there is the risk that such discussions could be misapplied to human social dynamics in ways that misrepresent biological phenomena.[95][96][97]

Applications Outside of Mammals

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While much of the research on the female masculinization hypothesis has focused on mammals, this concept has also been explored in other vertebrate and invertebrate species, where hormonal exposure during development can result in masculinized traits in females. Studies in birds, reptiles, amphibians, fish, and even some invertebrates have provided valuable insights into the broader applicability of the hypothesis and the role of androgens in shaping sexual differentiation across species.

A chukar partridge. In females of this species, elevated levels of androgens can lead to changes in aggression, territoriality, and courtship behaviors.

Birds

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In birds, particularly in species like domestic chickens (Gallus gallus domesticus) and chukars (Alectoris chukar), hormonal manipulation during early development has been shown to induce masculinized behaviors in females. In these species, elevated levels of androgens, such as testosterone, can lead to changes in aggression, territoriality, and courtship behaviors. For example, female chickens exposed to high levels of testosterone during embryonic development may display male-typical behaviors, such as increased aggression toward other females and more active participation in territorial defense. Similarly, in some species of quail, females exposed to elevated androgens show more dominant behaviors in social hierarchies and engage in competitive interactions usually associated with males.[98][99][100][101]

Research in birds has been instrumental in understanding the neuroendocrine mechanisms underlying sexual differentiation, particularly how early exposure to sex hormones can permanently alter the development of brain regions associated with behavior, including aggression and mating competition. These studies also demonstrate the flexibility of sexual behavior and the potential for females to express traits traditionally associated with males under certain hormonal conditions.[102][103][104]

A female Western mosquitofish. Females of this species have been hormonally manipulated in many scientific studies with androgens: masculinized females may compete with males for mates or display more dominant behaviors in social groups

Fish

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Fish species provide another diverse group where the female masculinization hypothesis has been applied. In species like the zebrafish (Danio rerio) and the mosquito fish (Gambusia affinis), researchers have manipulated hormonal exposure to examine its effects on female behavior and physiology. In some fish species, females exposed to elevated levels of androgens during development exhibit male-like traits, including increased aggression, territorial behavior, and changes in mate choice preferences. In the case of the mosquito fish, masculinized females may compete with males for mates or display more dominant behaviors in social groups.[105][106][107][108]

Additionally, fish are often used in studies on endocrine-disrupting chemicals (EDCs), which can lead to masculinized or feminized traits depending on the timing and level of exposure to environmental contaminants. These studies highlight the potential for EDCs to affect sexual differentiation in fish and the broader ecological consequences of widespread chemical pollutants on reproductive and social behaviors in aquatic environments.[109][110]

A Japanese wrinkled frog (Rana rugosa). Testosterone has been experimentally used to induce female frogs of this species to develop male-typical morphology.[111]

Amphibians

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The female masculinization hypothesis has also been explored in amphibians, particularly in species with environmental sex determination. In amphibians such as frogs and toads, elevated levels of androgens during critical periods of development can result in masculinized physical traits and altered mating behaviors in females. For example, in some species of frogs, females exposed to increased levels of testosterone can exhibit male-typical behaviors, such as increased aggression or competition for mates, and may even develop male-like reproductive organs.[112][113]

These studies contribute to our understanding of how environmental factors, such as temperature and hormonal exposure, interact to influence sexual differentiation in amphibians. They also highlight the potential for environmental stressors to disrupt the typical development of sexual traits in both males and females.[114][115][116]

A female green anole (Anolis carolinensis). Experimental treatment with androgens in females of this species leads to masculinized longer cartilages and larger dewlap muscle fibers.[117]

Reptiles

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In reptiles, particularly species with temperature-dependent sex determination (TSD) such as certain turtles and lizards, researchers have observed the impact of hormonal exposure on the masculinization of females. Although the primary determinant of sex in these species is temperature, additional exposure to androgens can masculinize females, influencing both physical traits and behavior. For example, in some species of lizards, females exposed to elevated androgen levels during their development may exhibit male-typical behaviors, including increased aggression and altered mating strategies.[118][119][120]

TSD species are especially interesting for studying the interaction between genetic, environmental, and hormonal factors in sexual differentiation, providing a unique context in which the female masculinization hypothesis can be tested. The role of hormonal exposure in these species also raises concerns about how climate change might influence sex ratios and behavioral patterns within reptile populations.[121][122]

A female fruit fly. Elevated androgen exposures in females of this species can result in exhibition of male-like behaviors, such as increased aggression or mating attempts toward other females

Invertebrates

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The female masculinization hypothesis has been explored in some invertebrate species, particularly in relation to hormonal control of sexual differentiation. In certain species of insects, such as the fruit fly (Drosophila melanogaster), exposure to sex hormones during development can influence the expression of male-typical traits in females. For example, in some cases, female fruit flies exposed to elevated levels of testosterone or other androgens during development may exhibit male-like behaviors, such as increased aggression or mating attempts toward other females.[123][124]

Research in invertebrates like fruit flies has also been instrumental in uncovering the genetic and molecular pathways through which hormones influence sexual differentiation. These studies offer a more detailed understanding of the mechanisms underlying masculinization and how they might be conserved across evolutionary lines.[125][126][127]

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The Challenge Hypothesis

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The Challenge Hypothesis, first proposed by Wingfield et al. in 1990, posits that testosterone levels in males are modulated by reproductive effort and social challenges, such as competition for mates or dominance. While traditionally applied to male behaviors, this hypothesis has increasingly been explored in the context of females, particularly in species where masculinized traits are observed.[128][129]

In females, the principles of the Challenge Hypothesis suggest that androgen levels may rise in response to competitive or reproductive pressures, leading to behaviors typically associated with males, such as aggression or territoriality. For example, in meerkats, dominant females exhibit elevated testosterone levels during periods of intense social competition, a pattern consistent with predictions from the Challenge Hypothesis. These hormonal surges may enhance traits like aggression and dominance, enabling females to maintain control over group dynamics and access to reproductive opportunities.[130][131]

The Female Masculinization Hypothesis extends this idea by examining how androgen exposure during prenatal or early developmental stages influences female behavior and physiology throughout life. The interaction between these two hypotheses provides a framework for understanding how short-term hormonal changes (as posited by the Challenge Hypothesis) and long-term developmental effects (central to the Female Masculinization Hypothesis) shape female behavior and reproductive strategies.[132][14]

However, some challenges arise when applying the Challenge Hypothesis to females. Unlike males, whose testosterone levels often show clear peaks during mating seasons or competitive encounters, the patterns in females can be more variable and context-dependent. Environmental factors, such as resource availability and social hierarchy, may play a more significant role in modulating androgen levels in females.[133]

Organizational versus activational effects of hormones during sexual development.

The Organizational-Activational Hypothesis

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The Organizational-Activational Hypothesis is a foundational framework in behavioral endocrinology, first proposed by Phoenix et al. in 1959. It posits that the effects of hormones on behavior occur in two distinct phases: an organizational phase during early development, when hormones shape the structure and function of the nervous system, and an activational phase later in life, when hormones influence behavior through transient effects.[134][135][136]

This hypothesis provides a critical context for understanding the Female Masculinization Hypothesis, as the Female Masculinization Hypothesis emphasizes the lasting impact of androgen exposure during early developmental windows on female physiology and behavior. According to the Female Masculinization Hypothesis, prenatal or neonatal exposure to elevated androgen levels can masculinize female traits, both physically and behaviorally. These organizational effects are thought to prime the individual for subsequent activational influences during adulthood, when hormonal changes further modulate behavior and reproductive strategies.[137][138]

For example, in rodents, exposure to testosterone in utero has been shown to masculinize brain structures and neural circuits associated with aggression and mating behavior. These organizational changes are later activated by hormonal surges during the reproductive phase, leading to behaviors typically associated with males, such as increased territoriality or dominance. Similarly, in spotted hyenas, androgen exposure during fetal development results in masculinized genitalia and increased aggression in females, behaviors that are further reinforced during adulthood by hormonal cycles.[139][140]

The Organizational-Activational Hypothesis also highlights the importance of timing and context in hormonal effects. Not all individuals exposed to androgens during development exhibit masculinized traits, suggesting that genetic background, environmental factors, and the presence of other hormones play significant roles in modulating these effects. This aligns with critiques of the Female Masculinization Hypothesis, which emphasize the complexity of hormonal environments and the need to consider broader ecological and social contexts.[141][142]

Maternal Androgen Effects

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The concept of maternal androgen effects highlights the influence of hormones produced by mothers during gestation on the development of their offspring. In many species, androgens such as testosterone can cross the placental barrier, affecting the growth, behavior, and reproductive strategies of the developing fetus. This phenomenon provides an important lens for understanding the Female Masculinisation Hypothesis, particularly regarding the prenatal androgen exposure believed to drive the masculinization of female traits.[143][144]

Research on maternal androgen effects suggests that elevated maternal androgen levels can have far-reaching developmental consequences. For example, in species such as rodents, increased maternal androgens during pregnancy have been linked to the development of masculinized traits in daughters, including altered genital morphology, increased aggression, and enhanced competitive behaviors. These traits often align with the predictions of the Female Masculinization Hypothesis, which posits that such masculinization can confer adaptive advantages under certain ecological or social conditions.[145][146][147]

In spotted hyenas, high maternal androgen levels are associated with the development of masculinized genitalia and social dominance in female offspring. These traits are thought to enhance the daughters’ reproductive success in the species’ highly competitive social structure. Similarly, in birds, maternal androgens deposited into egg yolks have been shown to influence offspring growth rates, aggression, and survival, demonstrating a broader relevance of maternal androgen effects beyond mammals.[148][149][150]

See more

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References

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  1. ^ Young, William C.; Goy, Robert W.; Phoenix, Charles H. (1964-01-17). "Hormones and Sexual Behavior". Science. 143 (3603): 212–218. Bibcode:1964Sci...143..212Y. doi:10.1126/science.143.3603.212. PMID 14077548.
  2. ^ Kruuk, H. (Hans) (1975). Hyaena. Internet Archive. London ; New York : Oxford University Press. ISBN 978-0-19-857395-1.
  3. ^ Kruuk, H. (Hans) (1974). The spotted hyena : a study of predation and social behavior. Internet Archive. Chicago : University of Chicago Press. ISBN 978-0-226-45507-5.
  4. ^ Glickman, S. E.; Frank, L. G.; Pavgi, S.; Licht, P. (1992-07-01). "Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity". Reproduction. 95 (2): 451–462. doi:10.1530/jrf.0.0950451. ISSN 0022-4251. PMID 1518001.
  5. ^ Baker, M.G. (1990) Effects of ovariectomy on dyadic aggression and submission in a colony of peripubertal spotted hyaenas (Crocuta crocuta). MA thesis, University of California, Berkeley.
  6. ^ Frank, L. G.; Glickman, S. E.; Powch, Irene (1990). "Sexual dimorphism in the spotted hyaena (Crocuta crocuta)". Journal of Zoology. 221 (2): 308–313. doi:10.1111/j.1469-7998.1990.tb04001.x. ISSN 1469-7998.
  7. ^ a b c Glickman, Stephen E.; Frank, Laurence G.; Licht, Paul; Yalcinkaya, Tamer; Siiteri, Pentti K.; Davidson, Julian (1992). "Sexual Differentiation of the Female Spotted Hyena". Annals of the New York Academy of Sciences. 662 (1): 135–159. Bibcode:1992NYASA.662..135G. doi:10.1111/j.1749-6632.1992.tb22858.x. ISSN 1749-6632.
  8. ^ a b Licht, P.; Frank, L. G.; Pavgi, S.; Yalcinkaya, T. M.; Siiteri, P. K.; Glickman, S. E. (1992-07-01). "Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta). 2. Maternal and fetal steroids". Reproduction. 95 (2): 463–474. doi:10.1530/jrf.0.0950463. ISSN 0022-4251. PMID 1518002.
  9. ^ Davies, Charli S.; Smyth, Kendra N.; Greene, Lydia K.; Walsh, Debbie A.; Mitchell, Jessica; Clutton-Brock, Tim; Drea, Christine M. (2016-10-18). "Exceptional endocrine profiles characterise the meerkat: sex, status, and reproductive patterns". Scientific Reports. 6 (1): 35492. Bibcode:2016NatSR...635492D. doi:10.1038/srep35492. ISSN 2045-2322. PMC 5067592. PMID 27752129.
  10. ^ "Sexual Selection Not Just for Males Anymore". phys.org. Retrieved 2025-01-02.
  11. ^ Johnstone, Rufus A.; Cant, Michael A.; Cram, Dominic; Thompson, Faye J. (2020-11-24). "Exploitative leaders incite intergroup warfare in a social mammal". Proceedings of the National Academy of Sciences. 117 (47): 29759–29766. Bibcode:2020PNAS..11729759J. doi:10.1073/pnas.2003745117. PMC 7703641. PMID 33168743.
  12. ^ a b Yalcinkaya, Tamer M.; Siiteri, Pentti K.; Vigne, Jean-Louis; Licht, Paul; Pavgi, Sushama; Frank, Laurence G.; Glickman, Stephen E. (1993-06-25). "A Mechanism for Virilization of Female Spotted Hyenas in Utero". Science. 260 (5116): 1929–1931. Bibcode:1993Sci...260.1929Y. doi:10.1126/science.8391165. PMID 8391165.
  13. ^ Glickman, Stephen E.; Cunha, Gerald R.; Drea, Christine M.; Conley, Alan J.; Place, Ned J. (2006-11-01). "Mammalian sexual differentiation: lessons from the spotted hyena". Trends in Endocrinology & Metabolism. 17 (9): 349–356. doi:10.1016/j.tem.2006.09.005. ISSN 1043-2760. PMID 17010637.
  14. ^ a b Drea, Christine M. (2009-08-01). "Endocrine Mediators of Masculinization in Female Mammals". Current Directions in Psychological Science. 18 (4): 221–226. doi:10.1111/j.1467-8721.2009.01640.x. ISSN 0963-7214.
  15. ^ Wilson, Edward O. (1975). Sociobiology : the new synthesis. Internet Archive. Cambridge, Mass. : Belknap Press of Harvard University Press. ISBN 978-0-674-81621-3.
  16. ^ Adkins-Regan, Elizabeth (2005). Hormones and animal social behavior. Internet Archive. Princeton : Princeton University Press. ISBN 978-0-691-09246-1.
  17. ^ Navara, Kristen J.; Nelson, Randy J. (2009-05-01). "Prenatal environmental influences on the production of sex-specific traits in mammals". Seminars in Cell & Developmental Biology. Environmental Regulation of Sex Dtermination in Vertebrates. 20 (3): 313–319. doi:10.1016/j.semcdb.2008.12.004. ISSN 1084-9521. PMID 19135541.
  18. ^ Drea, Christine M. (2005-11-01). "Bateman Revisited: The Reproductive Tactics of Female Primates1". Integrative and Comparative Biology. 45 (5): 915–923. doi:10.1093/icb/45.5.915. ISSN 1540-7063. PMID 21676842.
  19. ^ Eens, Marcel; Pinxten, Rianne (2000-10-05). "Sex-role reversal in vertebrates: behavioural and endocrinological accounts". Behavioural Processes. 51 (1): 135–147. doi:10.1016/S0376-6357(00)00124-8. ISSN 0376-6357. PMID 11074317.
  20. ^ Arnold, Arthur P. (2009-05-01). "The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 570–578. doi:10.1016/j.yhbeh.2009.03.011. ISSN 0018-506X. PMC 3671905. PMID 19446073.
  21. ^ Schulz, Kalynn M.; Molenda-Figueira, Heather A.; Sisk, Cheryl L. (2009-05-01). "Back to the future: The organizational-activational hypothesis adapted to puberty and adolescence". Hormones and Behavior. 55 (5): 597–604. doi:10.1016/j.yhbeh.2009.03.010. ISSN 1095-6867. PMC 2720102. PMID 19446076.
  22. ^ Cunha, Gerald R.; Risbridger, Gail; Wang, Hong; Place, Ned J.; Grumbach, Mel; Cunha, Tristan J.; Weldele, Mary; Conley, Al J.; Barcellos, Dale; Agarwal, Sanjana; Bhargava, Argun; Drea, Christine; Hammond, Geoffrey L.; Siiteri, Penti; Coscia, Elizabeth M. (2014). "Development of the external genitalia: perspectives from the spotted hyena (Crocuta crocuta)". Differentiation; Research in Biological Diversity. 87 (1–2): 4–22. doi:10.1016/j.diff.2013.12.003. ISSN 1432-0436. PMC 4069199. PMID 24582573.
  23. ^ Carlson, Anne A; Young, Andrew J; Russell, Andrew F; Bennett, Nigel C; McNeilly, Alan S; Clutton-Brock, Tim (2004-08-01). "Hormonal correlates of dominance in meerkats (Suricata suricatta)". Hormones and Behavior. 46 (2): 141–150. doi:10.1016/j.yhbeh.2004.01.009. ISSN 0018-506X. PMID 15256303.
  24. ^ de Luca, D. W.; Ginsberg, J. R. (2001-01-01). "Dominance, reproduction and survival in banded mongooses: towards an egalitarian social system?". Animal Behaviour. 61 (1): 17–30. doi:10.1006/anbe.2000.1559. ISSN 0003-3472. PMID 11170693.
  25. ^ Traish, Abdulmaged M; Kim, Noel; Min, Kweonsik; Munarriz, Ricardo; Goldstein, Irwin (2002-04-06). "Role of androgens in female genital sexual arousal: receptor expression, structure, and function". Fertility and Sterility. 77: 11–18. doi:10.1016/s0015-0282(02)02978-3. ISSN 0015-0282. PMID 12007897 – via Elsevier.
  26. ^ Crews, David (2008-06-01). "Epigenetics and its implications for behavioral neuroendocrinology". Frontiers in Neuroendocrinology. 29 (3): 344–357. doi:10.1016/j.yfrne.2008.01.003. ISSN 1095-6808. PMC 2394853. PMID 18358518.
  27. ^ a b Drea, Christine M. (2009-08-01). "Endocrine Mediators of Masculinization in Female Mammals". Current Directions in Psychological Science. 18 (4): 221–226. doi:10.1111/j.1467-8721.2009.01640.x. ISSN 0963-7214.
  28. ^ Zielinski, William J.; Vandenbergh, John G.; Montano, Monica M. (1991-01-01). "Effects of social stress and intrauterine position on sexual phenotype in wild-type house mice (Mus musculus)". Physiology & Behavior. 49 (1): 117–123. doi:10.1016/0031-9384(91)90241-F. ISSN 0031-9384. PMID 2017464.
  29. ^ Pellis, Sergio M.; Pellis, Vivien C.; McKenna, Mario M. (1994). "Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens". Journal of Comparative Psychology. 108 (1): 68–73. doi:10.1037/0735-7036.108.1.68. ISSN 1939-2087. PMID 8174346.
  30. ^ Quadagno, D. M.; Shryne, J.; Anderson, C.; Gorski, R. A. (1972-11-01). "Influence of gonadal hormones on social, sexual, emergence, and open field behaviour in the rat (Rattus norvegicus)". Animal Behaviour. 20 (4): 732–740. doi:10.1016/S0003-3472(72)80145-3. ISSN 0003-3472. PMID 4661317.
  31. ^ Chu, Xi; Snoeren, Eelke; Södersten, Per; Ågmo, Anders (2021-08-01). "Sexual incentive motivation and male and female copulatory behavior in female rats given androgen from postnatal day 20". Physiology & Behavior. 237: 113460. doi:10.1016/j.physbeh.2021.113460. ISSN 0031-9384. PMID 33991538.
  32. ^ Saunders, Paul A.; Franco, Thomas; Sottas, Camille; Maurice, Tangui; Ganem, Guila; Veyrunes, Frédéric (2016-03-11). "Masculinised Behaviour of XY Females in a Mammal with Naturally Occurring Sex Reversal". Scientific Reports. 6 (1): 22881. Bibcode:2016NatSR...622881S. doi:10.1038/srep22881. ISSN 2045-2322.
  33. ^ Biancardi, Manoel F.; Perez, Ana P. S.; Caires, Cássia Regina Suzuki; Góes, Rejane M.; Vilamaior, Patrícia S. L.; Santos, Fernanda C. A.; Taboga, Sebastião R. (2015-09-14). "Prenatal exposure to testosterone masculinises the female gerbil and promotes the development of lesions in the prostate (Skene's gland)". Reproduction, Fertility and Development. 27 (7): 1000–1011. doi:10.1071/RD13387. ISSN 1448-5990. PMID 25483231.
  34. ^ Tomaszycki, Michelle L.; Gouzoules, Harold; Wallen, Kim (2005). "Sex differences in juvenile rhesus macaque (Macaca mulatta) agonistic screams: Life history differences and effects of prenatal androgens". Developmental Psychobiology. 47 (4): 318–327. doi:10.1002/dev.20102. ISSN 1098-2302. PMID 16284962.
  35. ^ Hemelrijk, Charlotte K.; Wantia, Jan; Isler, Karin (2008-07-16). "Female Dominance over Males in Primates: Self-Organisation and Sexual Dimorphism". PLOS ONE. 3 (7): e2678. Bibcode:2008PLoSO...3.2678H. doi:10.1371/journal.pone.0002678. ISSN 1932-6203. PMC 2441829. PMID 18628830.
  36. ^ Zehr, Julia L.; Van Meter, Page E.; Wallen, Kim (2005-05-01). "Factors Regulating the Timing of Puberty Onset in Female Rhesus Monkeys (Macaca mulatta): Role of Prenatal Androgens, Social Rank, and Adolescent Body Weight1". Biology of Reproduction. 72 (5): 1087–1094. doi:10.1095/biolreprod.104.027755. ISSN 0006-3363. PMID 15625235.
  37. ^ Wrangham, R. W. (1981-08-01). "Drinking competition in vervet monkeys". Animal Behaviour. 29 (3): 904–910. doi:10.1016/S0003-3472(81)80027-9. ISSN 0003-3472.
  38. ^ Wallen, K.; Hassett, J. M. (2009). "Sexual Differentiation of Behaviour in Monkeys: Role of Prenatal Hormones". Journal of Neuroendocrinology. 21 (4): 421–426. doi:10.1111/j.1365-2826.2009.01832.x. ISSN 1365-2826. PMC 2704567. PMID 19207815.
  39. ^ McFadden, Dennis; Pasanen, Edward G.; Valero, Michelle D.; Roberts, Eila K.; Lee, Theresa M. (2009-01-01). "Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep (Ovis aries)". Hormones and Behavior. 55 (1): 98–105. doi:10.1016/j.yhbeh.2008.08.013. ISSN 0018-506X. PMC 2649662. PMID 18834887.
  40. ^ Vázquez, Reyes; Orihuela, Agustín; Aguirre, Virginio (2014-05-01). "A note on the effect of number (single or twin) and sex of contemporary siblings on male-like play behavior of lambs (Ovis aries)". Journal of Veterinary Behavior. 9 (3): 132–135. doi:10.1016/j.jveb.2014.01.003. ISSN 1558-7878.
  41. ^ Roberts, Eila K.; Padmanabhan, Vasantha; Lee, Theresa M. (2008-07-01). "Differential Effects of Prenatal Testosterone Timing and Duration on Phenotypic and Behavioral Masculinization and Defeminization of Female Sheep1". Biology of Reproduction. 79 (1): 43–50. doi:10.1095/biolreprod.107.067074. ISSN 0006-3363.
  42. ^ Popescu, PAUL C. (1990-01-01), McFeely, Richard A. (ed.), "Chromosomes of the Cow and Bull", Advances in Veterinary Science and Comparative Medicine, Domestic Animal Cytogenetics, vol. 34, Academic Press, pp. 41–71, doi:10.1016/b978-0-12-039234-6.50007-0, ISBN 978-0-12-039234-6, retrieved 2025-01-02
  43. ^ Graïc, Jean-Marie; Corain, Livio; Peruffo, Antonella; Cozzi, Bruno; Swaab, Dick F. (2018). "The bovine anterior hypothalamus: Characterization of the vasopressin–oxytocin containing nucleus and changes in relation to sexual differentiation". Journal of Comparative Neurology. 526 (17): 2898–2917. doi:10.1002/cne.24542. ISSN 1096-9861. PMID 30255945.
  44. ^ Pavlicev, Mihaela; Herdina, Anna Nele; Wagner, Günter (2022-09-01). "Female Genital Variation Far Exceeds That of Male Genitalia: A Review of Comparative Anatomy of Clitoris and the Female Lower Reproductive Tract in Theria". Integrative and Comparative Biology. 62 (3): 581–601. doi:10.1093/icb/icac026. ISSN 1540-7063. PMC 9494530. PMID 35524696.
  45. ^ Conservation of endangered species in captivity : an interdisciplinary approach. Internet Archive. Albany, N.Y. : State University of New York Press. 1995. ISBN 978-0-7914-1911-3.{{cite book}}: CS1 maint: others (link)
  46. ^ Kunz, Thomas H.; Hood, Wendy R. (2000-01-01), Crichton, Elizabeth G.; Krutzsch, Philip H. (eds.), "10 - Parental Care and Postnatal Growth in the Chiroptera", Reproductive Biology of Bats, London: Academic Press, pp. 415–468, doi:10.1016/b978-012195670-7/50011-4, ISBN 978-0-12-195670-7, retrieved 2025-01-02
  47. ^ Drake, Gabrielle Jeanne-Clare; Cowl, Veronica; Ashpole, Ian; Rowland, Hannah; White, David; McDonald, Monica; Chantrey, Julian; Lopez, Javier; Feltrer-Rambaud, Yedra (2021-10-31). "The use of etonogestrel (Nexplanon®) and aglepristone (Alizin®) for population management of a colony of Rodrigues fruit bats (Pteropus rodricensis)". Journal of Zoo and Aquarium Research. 9 (4): 239–246. doi:10.19227/jzar.v9i4.627. ISSN 2214-7594.
  48. ^ Signoret, J. P. (1993), Haug, Marc; Whalen, Richard E.; Aron, Claude; Olsen, Kathie L. (eds.), "Sexualisation of Behavior During Development in the Pig", The Development of Sex Differences and Similarities in Behavior, Dordrecht: Springer Netherlands, pp. 279–289, doi:10.1007/978-94-011-1709-8_16, ISBN 978-94-011-1709-8, retrieved 2025-01-02
  49. ^ Geijer-Simpson, Annika Vera (2022-04-22). The sex biased litter in utero and its effect on post-natal health, development, and reproductive capacity of the commercial pig (phd thesis). University of Leeds.
  50. ^ Park, Jin Ho; Rissman, Emilie F. (2011-01-01), Norris, David O.; Lopez, Kristin H. (eds.), "Chapter 8 - Behavioral Neuroendocrinology of Reproduction in Mammals", Hormones and Reproduction of Vertebrates, London: Academic Press, pp. 139–173, doi:10.1016/b978-0-12-374928-4.10008-2, ISBN 978-0-12-374928-4, retrieved 2025-01-02
  51. ^ Emlen, Stephen T.; Oring, Lewis W. (1977). "Ecology, Sexual Selection, and the Evolution of Mating Systems". Science. 197 (4300): 215–223. Bibcode:1977Sci...197..215E. doi:10.1126/science.327542. ISSN 0036-8075. JSTOR 1744497. PMID 327542.
  52. ^ Kauffman, Alexander S.; Micevych, Paul E. (2019-01-01), "Female Sexual Behavior and Hormones in Mammals☆", in Choe, Jae Chun (ed.), Encyclopedia of Animal Behavior (Second Edition), Oxford: Academic Press, pp. 403–419, doi:10.1016/b978-0-12-809633-8.20687-0, ISBN 978-0-12-813252-4, retrieved 2025-01-02
  53. ^ Sharma, Usha R.; Rissman, Emilie F. (1994). "Testosterone Implants in Specific Neural Sites Activate Female Sexual Behaviour". Journal of Neuroendocrinology. 6 (4): 423–432. doi:10.1111/j.1365-2826.1994.tb00603.x. ISSN 1365-2826. PMID 7987373.
  54. ^ Sciences (US), National Academy of; Avise, John C.; Ayala, Francisco J. (2009), "Sexual Selection and Mating Systems", In the Light of Evolution: Volume III: Two Centuries of Darwin, National Academies Press (US), retrieved 2025-01-02
  55. ^ Wong, Bob B. M.; Candolin, Ulrika (2005). "How is female mate choice affected by male competition?". Biological Reviews. 80 (4): 559–571. doi:10.1017/S1464793105006809. hdl:1912/256. ISSN 1469-185X. PMID 16221329.
  56. ^ Amundsen, Trond (2018-06-01). "Sex roles and sexual selection: lessons from a dynamic model system". Current Zoology. 64 (3): 363–392. doi:10.1093/cz/zoy036. ISSN 2396-9814. PMC 6007278. PMID 30402079.
  57. ^ "Sexual Selection | Princeton University Press". press.princeton.edu. 1994-06-16. Retrieved 2025-01-02.
  58. ^ Reproductive success : studies of individual variation in contrasting breeding systems. Internet Archive. Chicago : University of Chicago Press. 1988. ISBN 978-0-226-11058-5.{{cite book}}: CS1 maint: others (link)
  59. ^ Berglund, Anders; Bisazza, Angelo; Pilastro, Andrea (1996-08-01). "Armaments and ornaments: an evolutionary explanation of traits of dual utility". Biological Journal of the Linnean Society. 58 (4): 385–399. doi:10.1111/j.1095-8312.1996.tb01442.x. ISSN 0024-4066.
  60. ^ Hangartner, Sandra; Sgrò, Carla M.; Connallon, Tim; Booksmythe, Isobel (2022). "Sexual dimorphism in phenotypic plasticity and persistence under environmental change: An extension of theory and meta-analysis of current data". Ecology Letters. 25 (6): 1550–1565. Bibcode:2022EcolL..25.1550H. doi:10.1111/ele.14005. ISSN 1461-0248. PMC 9311083. PMID 35334155.
  61. ^ Fox, Rebecca J.; Fromhage, Lutz; Jennions, Michael D. (2019-01-28). "Sexual selection, phenotypic plasticity and female reproductive output". Philosophical Transactions of the Royal Society B: Biological Sciences. 374 (1768): 20180184. doi:10.1098/rstb.2018.0184. PMC 6365872. PMID 30966965.
  62. ^ Vilas, Julia Sanchez (2018-01-01). "Sexual dimorphism in response to stress". Environmental and Experimental Botany. 146: 1. Bibcode:2018EnvEB.146....1R. doi:10.1016/j.envexpbot.2017.12.006. hdl:10347/16235.
  63. ^ Hines, Melissa; Constantinescu, Mihaela; Spencer, Debra (2015). "Early androgen exposure and human gender development". Biology of Sex Differences. 6: 3. doi:10.1186/s13293-015-0022-1. ISSN 2042-6410. PMC 4350266. PMID 25745554.
  64. ^ Tenugu, Swathi; Senthilkumaran, Balasubramanian (2022-09-01). "Sexual plasticity in bony fishes: Analyzing morphological to molecular changes of sex reversal". Aquaculture and Fisheries. Reproduction and Gonadal Development in Bony Fishes. 7 (5): 525–539. Bibcode:2022AqFis...7..525T. doi:10.1016/j.aaf.2022.02.007. ISSN 2468-550X.
  65. ^ Toppari, Jorma; Skakkeb˦k, Niels E. (1998-04-01). "Sexual differentiation and environmental endocrine disrupters". Baillière's Clinical Endocrinology and Metabolism. 12 (1): 143–156. doi:10.1016/S0950-351X(98)80529-6. ISSN 0950-351X. PMID 9890066.
  66. ^ Patisaul, Heather B.; Adewale, Heather B. (2009-06-29). "Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior". Frontiers in Behavioral Neuroscience. 3. doi:10.3389/neuro.08.010.2009. ISSN 1662-5153. PMC 2706654. PMID 19587848.
  67. ^ McWhinnie, Kirsty; Negi, Deepti; Tanner, K. Elizabeth; Parsons, Kevin J. (2023-11-28). "Functional trait plasticity diverges between sexes in African cichlids: A contribution toward ecological sexual dimorphism?". Ecology and Evolution. 13 (11): e10702. Bibcode:2023EcoEv..1310702M. doi:10.1002/ece3.10702. ISSN 2045-7758. PMID 38034329 – via PMC.
  68. ^ Novak, Sara. "Females Dominate Males in Many Primate Species". Scientific American. Retrieved 2025-01-02.
  69. ^ Hemelrijk, Charlotte K.; Wantia, Jan; Isler, Karin (2008-07-16). "Female dominance over males in primates: self-organisation and sexual dimorphism". PLOS ONE. 3 (7): e2678. Bibcode:2008PLoSO...3.2678H. doi:10.1371/journal.pone.0002678. ISSN 1932-6203. PMC 2441829. PMID 18628830.
  70. ^ Lewis, Rebecca J. (2018). "Female Power in Primates and the Phenomenon of Female Dominance". Annual Review of Anthropology. 47: 533–551. doi:10.1146/annurev-anthro-102317-045958. ISSN 0084-6570. JSTOR 48550921.
  71. ^ Waal, Frans de (2014-09-01). "Why Humans and Other Primates Cooperate". Scientific American. Retrieved 2025-01-02.
  72. ^ Robinson, Elva J. H.; Barker, Jessica L. (2017-03-01). "Inter-group cooperation in humans and other animals". Biology Letters. 13 (3): 20160793. doi:10.1098/rsbl.2016.0793. PMC 5377026. PMID 28250206.
  73. ^ Bertram, Brian C. R. (1975). "The Social System of Lions". Scientific American. 232 (5): 54–65. Bibcode:1975SciAm.232e..54B. doi:10.1038/scientificamerican0575-54. ISSN 0036-8733. JSTOR 24949799.
  74. ^ "Parental Investment and Sexual Selection". ResearchGate. Archived from the original on 2023-12-11. Retrieved 2025-01-02.
  75. ^ Klug, Hope; Bonsall, Michael B. (2010-03-01). "Life History and the Evolution of Parental Care". Evolution. 64 (3): 823–835. doi:10.1111/j.1558-5646.2009.00854.x. ISSN 0014-3820. PMID 19796144.
  76. ^ Rymer, T. L.; Pillay, N. (2018). "An integrated understanding of paternal care in mammals: lessons from the rodents". Journal of Zoology. 306 (2): 69–76. doi:10.1111/jzo.12575. ISSN 1469-7998.
  77. ^ Wynne-Edwards, Katherine E. (2001-09-01). "Hormonal Changes in Mammalian Fathers". Hormones and Behavior. 40 (2): 139–145. doi:10.1006/hbeh.2001.1699. ISSN 0018-506X. PMID 11534974.
  78. ^ McEwen, Bruce S.; Milner, Teresa A. (2017-01-02). "Understanding the broad influence of sex hormones and sex differences in the brain". Journal of Neuroscience Research. 95 (1–2): 24–39. doi:10.1002/jnr.23809. ISSN 1097-4547. PMC 5120618. PMID 27870427.
  79. ^ Negri-Cesi, P.; Colciago, A.; Celotti, F.; Motta, M. (2004). "Sexual differentiation of the brain: role of testosterone and its active metabolites". Journal of Endocrinological Investigation. 27 (6 Suppl): 120–127. ISSN 0391-4097. PMID 15481811.
  80. ^ Balthazart, Jacques (2019-10-01). "New concepts in the study of the sexual differentiation and activation of reproductive behavior, a personal view". Frontiers in Neuroendocrinology. 55: 100785. doi:10.1016/j.yfrne.2019.100785. ISSN 1095-6808. PMC 6858558. PMID 31430485.
  81. ^ Matsushita, Shoko; Suzuki, Kentaro; Murashima, Aki; Kajioka, Daiki; Acebedo, Alvin Resultay; Miyagawa, Shinichi; Haraguchi, Ryuma; Ogino, Yukiko; Yamada, Gen (2018-06-18). "Regulation of masculinization: androgen signalling for external genitalia development". Nature Reviews Urology. 15 (6): 358–368. doi:10.1038/s41585-018-0008-y. ISSN 1759-4820. PMID 29670181.
  82. ^ "Hormones and neuroplasticity: A lifetime of... : Neuroscience and Biobehavioral Reviews". Ovid. doi:10.1016/j.neubiorev.2021.11.029~hormones-and-neuroplasticity-a-lifetime-of-adaptive (inactive 2 January 2025). Retrieved 2025-01-02.{{cite web}}: CS1 maint: DOI inactive as of January 2025 (link)
  83. ^ Hau, Michaela; Goymann, Wolfgang (2015-08-24). "Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions". Frontiers in Zoology. 12 (1): S7. doi:10.1186/1742-9994-12-S1-S7. ISSN 1742-9994. PMC 4722346. PMID 26816524.
  84. ^ Holekamp, Kay E; Strauss, Eli D (2016-12-01). "Aggression and dominance: an interdisciplinary overview". Current Opinion in Behavioral Sciences. Behavioral ecology. 12: 44–51. doi:10.1016/j.cobeha.2016.08.005. ISSN 2352-1546.
  85. ^ Sjoberg, Espen A. (2017-02-15). "Logical fallacies in animal model research". Behavioral and Brain Functions. 13 (1): 3. doi:10.1186/s12993-017-0121-8. ISSN 1744-9081. PMC 5312558. PMID 28202023.
  86. ^ Barroca, Nayara Cobra Barreiro; Della Santa, Giovanna; Suchecki, Deborah; García-Cairasco, Norberto; Umeoka, Eduardo Henrique de Lima (2022-09-01). "Challenges in the use of animal models and perspectives for a translational view of stress and psychopathologies". Neuroscience & Biobehavioral Reviews. 140: 104771. doi:10.1016/j.neubiorev.2022.104771. ISSN 0149-7634. PMID 35817171.
  87. ^ DeWitt, Thomas J; Scheiner, Samuel M, eds. (2004-01-15). Phenotypic Plasticity. Oxford University PressNew York, NY. doi:10.1093/oso/9780195138962.001.0001. ISBN 978-0-19-513896-2.
  88. ^ Kaiser, Sylvia; Hennessy, Michael B.; Sachser, Norbert (2015-08-24). "Domestication affects the structure, development and stability of biobehavioural profiles". Frontiers in Zoology. 12 (1): S19. doi:10.1186/1742-9994-12-S1-S19. ISSN 1742-9994. PMC 5385816. PMID 28400853.
  89. ^ Stokes, William S.; Marsman, Daniel S. (2014-01-01), Bayne, Kathryn; Turner, Patricia V. (eds.), "Chapter 9 - Animal Welfare Considerations in Biomedical Research and Testing", Laboratory Animal Welfare, American College of Laboratory Animal Medicine, Boston: Academic Press, pp. 115–140, doi:10.1016/b978-0-12-385103-1.00009-9, ISBN 978-0-12-385103-1, retrieved 2025-01-02
  90. ^ Patisaul, Heather B.; Fenton, Suzanne E.; Aylor, David (2018-06-01). "Animal models of endocrine disruption". Best Practice & Research. Clinical Endocrinology & Metabolism. 32 (3): 283–297. doi:10.1016/j.beem.2018.03.011. ISSN 1878-1594. PMC 6029710. PMID 29779582.
  91. ^ Qaid, Mohammed M.; Abdoun, Khalid A. (2022-12-31). "Safety and concerns of hormonal application in farm animal production: a review". Journal of Applied Animal Research. 50 (1): 426–439. doi:10.1080/09712119.2022.2089149. ISSN 0971-2119 – via Tandfonline.
  92. ^ Davies, William; Wilkinson, Lawrence S. (2006-12-18). "It is not all hormones: Alternative explanations for sexual differentiation of the brain". Brain Research. Sex, Genes and Steroids. 1126 (1): 36–45. doi:10.1016/j.brainres.2006.09.105. ISSN 0006-8993.
  93. ^ Shine, Richard (1989). "Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence". The Quarterly Review of Biology. 64 (4): 419–461. doi:10.1086/416458. ISSN 0033-5770. JSTOR 2830103. PMID 2697022.
  94. ^ Kappeler, Peter M.; Benhaiem, Sarah; Fichtel, Claudia; Fromhage, Lutz; Höner, Oliver P.; Jennions, Michael D.; Kaiser, Sylvia; Krüger, Oliver; Schneider, Jutta M.; Tuni, Cristina; van Schaik, Jaap; Goymann, Wolfgang (2023). "Sex roles and sex ratios in animals". Biological Reviews. 98 (2): 462–480. doi:10.1111/brv.12915. ISSN 1469-185X. PMID 36307924.
  95. ^ Differences, Institute of Medicine (US) Committee on Understanding the Biology of Sex and Gender; Wizemann, Theresa M.; Pardue, Mary-Lou (2001), "The Future of Research on Biological Sex Differences: Challenges and Opportunities", Exploring the Biological Contributions to Human Health: Does Sex Matter?, National Academies Press (US), retrieved 2025-01-02
  96. ^ Roselli, C. E. (2018). "Neurobiology of gender identity and sexual orientation". Journal of Neuroendocrinology. 30 (7): e12562. doi:10.1111/jne.12562. ISSN 1365-2826. PMC 6677266. PMID 29211317.
  97. ^ Wood, Wendy; Eagly, Alice H. (2012-01-01), Olson, James M.; Zanna, Mark P. (eds.), "Chapter two - Biosocial Construction of Sex Differences and Similarities in Behavior", Advances in Experimental Social Psychology, vol. 46, Academic Press, pp. 55–123, doi:10.1016/b978-0-12-394281-4.00002-7, retrieved 2025-01-02
  98. ^ Kent, John P.; Hynes, Niamh M.; Hayden, Thomas J.; Murphy, Kenneth J.; O'Dywer, Laurence (2018-06-20). Hens (Gallus gallus domesticus) with larger spurs have higher faecal testosterone levels; evidence of female to male - like phenotype (Report). PeerJ Preprints.
  99. ^ Jessl, Luzie; Lenz, Rebecca; Massing, Fabian G.; Scheider, Jessica; Oehlmann, Jörg (2018-07-03). "Effects of estrogens and antiestrogens on gonadal sex differentiation and embryonic development in the domestic fowl (Gallus gallus domesticus)". PeerJ. 6: e5094. doi:10.7717/peerj.5094. ISSN 2167-8359. PMC 6034593. PMID 30002959.
  100. ^ West, J. L. (1974). "Case Report: Arrhenoblastoma in a Chukar Partridge". Avian Diseases. 18 (2): 258–261. doi:10.2307/1589136. ISSN 0005-2086. JSTOR 1589136.
  101. ^ Adkins-Regan, Elizabeth (1985-08-01). "Exposure of embryos to an aromatization inhibitor increases copulatory behaviour of male quail". Behavioural Processes. 11 (2): 153–158. doi:10.1016/0376-6357(85)90056-7. ISSN 0376-6357. PMID 24895921.
  102. ^ Paster, Michael B. (1991-11-01). "Avian Reproductive Endocrinology". Veterinary Clinics of North America: Small Animal Practice. 21 (6): 1343–1359. doi:10.1016/S0195-5616(91)50143-1. ISSN 0195-5616. PMID 1767479.
  103. ^ Major, Andrew T.; Smith, Craig A. (2016-08-17). "Sex Reversal in Birds". Sexual Development. 10 (5–6): 288–300. doi:10.1159/000448365. ISSN 1661-5425. PMID 27529790.
  104. ^ Arnold, Arthur P.; Itoh, Yuichiro (2011-07-01). "Factors Causing Sex differences in Birds". Avian Biology Research. 4 (2): 44–51. doi:10.3184/175815511X13070045977959. ISSN 1758-1559. PMC 3864897. PMID 24353746.
  105. ^ Lee, Stephanie L J; Horsfield, Julia A; Black, Michael A; Rutherford, Kim; Gemmell, Neil J (2018-08-01). "Identification of sex differences in zebrafish (Danio rerio) brains during early sexual differentiation and masculinization using 17α-methyltestoterone†". Biology of Reproduction. 99 (2): 446–460. doi:10.1093/biolre/iox175. ISSN 0006-3363. PMID 29272338.
  106. ^ Chen, Lu; Wang, Li; Cheng, Qiwei; Tu, Yi-Xuan; Yang, Zhuang; Li, Run-Ze; Luo, Zhi-Hui; Chen, Zhen-Xia (2020-01-07). "Anti-masculinization induced by aromatase inhibitors in adult female zebrafish". BMC Genomics. 21 (1): 22. doi:10.1186/s12864-019-6437-z. ISSN 1471-2164. PMC 6947999. PMID 31910818.
  107. ^ Hou, Li-Ping; Yang, Yang; Shu, Hu; Ying, Guang-Guo; Zhao, Jian-Liang; Fang, Gui-Zhen; Xin, Li; Shi, Wen-Jun; Yao, Li; Cheng, Xue-Mei (2018-01-01). "Masculinization and reproductive effects in western mosquitofish (Gambusia affinis) after long-term exposure to androstenedione". Ecotoxicology and Environmental Safety. 147: 509–515. Bibcode:2018EcoES.147..509H. doi:10.1016/j.ecoenv.2017.08.004. ISSN 0147-6513. PMID 28915398.
  108. ^ Deaton, Raelynn; Cureton, James C. (2011-12-01). "Female masculinization and reproductive life history in the western mosquitofish (Gambusia affinis)". Environmental Biology of Fishes. 92 (4): 551–558. Bibcode:2011EnvBF..92..551D. doi:10.1007/s10641-011-9878-z. ISSN 1573-5133.
  109. ^ Baumann, Lisa; Knörr, Susanne; Keiter, Susanne; Nagel, Tina; Segner, Helmut; Braunbeck, Thomas (2015-11-01). "Prochloraz causes irreversible masculinization of zebrafish (Danio rerio)". Environmental Science and Pollution Research. 22 (21): 16417–16422. Bibcode:2015ESPR...2216417B. doi:10.1007/s11356-014-3486-3. ISSN 1614-7499. PMID 25163568.
  110. ^ Hou, Liping; Chen, Shangduo; Chen, Hongxing; Ying, Guangguo; Chen, Diyun; Liu, Juan; Liang, Ye; Wu, Rongrong; Fang, Xuwen; Zhang, Cuiping; Xie, Lingtian (2019-02-01). "Rapid masculinization and effects on the liver of female western mosquitofish (Gambusia affinis) by norethindrone". Chemosphere. 216: 94–102. Bibcode:2019Chmsp.216...94H. doi:10.1016/j.chemosphere.2018.10.130. ISSN 0045-6535. PMID 30359922.
  111. ^ Oike, Akira; Kodama, Maho; Nakamura, Yoriko; Nakamura, Masahisa (2016). "A Threshold Dosage of Testosterone for Female-to-Male Sex Reversal in Rana rugosa Frogs". Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. 325 (8): 532–538. Bibcode:2016JEZA..325..532O. doi:10.1002/jez.2037. ISSN 1932-5231. PMID 27677985.
  112. ^ Eggert, Christophe (2004-11-01). "Sex determination: the amphibian models". Reproduction Nutrition Development. 44 (6): 539–549. doi:10.1051/rnd:2004062. ISSN 0926-5287. PMID 15762298.
  113. ^ Wallace, H.; Badawy, G. M. I.; Wallace, B. M. N. (1999-06-01). "Amphibian sex determination and sex reversal". Cellular and Molecular Life Sciences CMLS. 55 (6): 901–909. doi:10.1007/s000180050343. ISSN 1420-9071. PMC 11147005. PMID 10412371.
  114. ^ Orton, Frances; Tyler, Charles R. (2015). "Do hormone-modulating chemicals impact on reproduction and development of wild amphibians?". Biological Reviews. 90 (4): 1100–1117. doi:10.1111/brv.12147. ISSN 1469-185X. PMID 25335651.
  115. ^ Archer, Edward (2014-04-16). Androgen controlled secondary sexual characters in the male African clawed frog, Xenopus laevis, as potential biomarkers for endocrine disruptor contaminants (with special reference to fungicides) in aquatic systems (Thesis). Stellenbosch : Stellenbosch University.
  116. ^ Wallace, H.; Wallace, B. M. (2000-10-01). "Sex reversal of the newt Triturus cristatus reared at extreme temperatures". The International Journal of Developmental Biology. 44 (7): 807–810. ISSN 0214-6282. PMID 11128575.
  117. ^ Lovern, Matthew B; Holmes, Melissa M; Fuller, Carly O; Wade, Juli (2004-05-01). "Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles (Anolis carolinensis)". Hormones and Behavior. 45 (5): 295–305. doi:10.1016/j.yhbeh.2003.10.003. ISSN 0018-506X. PMID 15109903.
  118. ^ Ehl, Jan; Vukić, Jasna; Kratochvíl, Lukáš (2017-11-01). "Hormonal and thermal induction of sex reversal in the bearded dragon (Pogona vitticeps, Agamidae)". Zoologischer Anzeiger. 271: 1–5. Bibcode:2017ZooAn.271....1E. doi:10.1016/j.jcz.2017.11.002. ISSN 0044-5231.
  119. ^ Milnes, Matthew R.; Robinson, Christopher D.; Foley, Alexis P.; Stepp, Charleigh; Hale, Matthew D.; John-Alder, Henry B.; Cox, Robert M. (2024-01-15). "Effects of testosterone on urogenital tract morphology and androgen receptor expression in immature Eastern Fence lizards (Sceloporus undulatus)". General and Comparative Endocrinology. 346: 114418. doi:10.1016/j.ygcen.2023.114418. ISSN 0016-6480. PMID 38036014.
  120. ^ Holleley, Clare E.; Sarre, Stephen D.; O'Meally, Denis; Georges, Arthur (2016-10-29). "Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change?". Sexual Development. 10 (5–6): 279–287. doi:10.1159/000450972. ISSN 1661-5425. PMID 27794577.
  121. ^ Dutton, P. H.; Whitmore, C. P.; Mrosovsky, N. (1985-01-01). "Masculinisation of leatherback turtle Dermochelys coriacea hatchlings from eggs incubated in styrofoam boxes". Biological Conservation. 31 (3): 249–264. Bibcode:1985BCons..31..249D. doi:10.1016/0006-3207(85)90070-9. ISSN 0006-3207.
  122. ^ Stubbs, Jessica L.; Kearney, Michael R.; Whiting, Scott D.; Mitchell, Nicola J. (2014-10-22). "Models of primary sex ratios at a major flatback turtle rookery show an anomalous masculinising trend". Climate Change Responses. 1 (1): 3. Bibcode:2014ClChR...1....3S. doi:10.1186/s40665-014-0003-3. ISSN 2053-7565.
  123. ^ Monyak, Rachel E.; Golbari, Nicole M.; Chan, Yick-Bun; Pranevicius, Ausra; Tang, Grace; Fernández, Maria Paz; Kravitz, Edward A. (2021-03-25). "Masculinized Drosophila females adapt their fighting strategies to their opponent". Journal of Experimental Biology. 224 (6): jeb238006. Bibcode:2021JExpB.224B8006M. doi:10.1242/jeb.238006. ISSN 0022-0949. PMC 8015213. PMID 33568440.
  124. ^ Slee, Roger; Bownes, Mary (1990-06-01). "Sex Determination in Drosophila melanogaster". The Quarterly Review of Biology. 65 (2): 175–204. doi:10.1086/416718. ISSN 0033-5770. PMID 2117298.
  125. ^ Juchault, P; Louis, C; Martin, G; Noulin, G (1991-12-01). "Masculinization of female isopods (Crustacea) correlated with non-Mendelian inheritance of cytoplasmic viruses". Proceedings of the National Academy of Sciences. 88 (23): 10460–10464. Bibcode:1991PNAS...8810460J. doi:10.1073/pnas.88.23.10460. PMC 52948. PMID 11607243.
  126. ^ Ford, Alex T.; Fernandes, Teresa F.; Rider, Sebastien A.; Read, Paul A.; Robinson, Craig D.; Davies, Ian M. (2004-08-01). "Endocrine disruption in a marine amphipod? Field observations of intersexuality and de-masculinisation". Marine Environmental Research. Twelfth International Symposium on Pollutant Responses in Marine Organisms. 58 (2): 169–173. Bibcode:2004MarER..58..169F. doi:10.1016/j.marenvres.2004.03.013. ISSN 0141-1136. PMID 15178030.
  127. ^ Langston, W. J. (2020-06-30). "Endocrine disruption and altered sexual development in aquatic organisms: an invertebrate perspective". Journal of the Marine Biological Association of the United Kingdom. 100 (4): 495–515. Bibcode:2020JMBUK.100..495L. doi:10.1017/S0025315420000533. ISSN 0025-3154.
  128. ^ Wingfield, John C. (2017-06-01). "The challenge hypothesis: Where it began and relevance to humans". Hormones and Behavior. Hormones and Human Competition. 92: 9–12. doi:10.1016/j.yhbeh.2016.11.008. ISSN 0018-506X. PMID 27856292.
  129. ^ Wingfield, John C.; Hegner, Robert E.; Dufty, Alfred M.; Ball, Gregory F. (1990-12-01). "The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies". The American Naturalist. 136 (6): 829–846. Bibcode:1990ANat..136..829W. doi:10.1086/285134. ISSN 0003-0147.
  130. ^ Goymann, Wolfgang; Moore, Ignacio T.; Oliveira, Rui F. (2019). "Challenge Hypothesis 2.0: A Fresh Look at an Established Idea". BioScience. 69 (6): 432–442. doi:10.1093/biosci/biz041. ISSN 0006-3568. JSTOR 26732562.
  131. ^ Drea, Christine M.; Davies, Charli S. (2022-09-01). "Meerkat manners: Endocrine mediation of female dominance and reproductive control in a cooperative breeder". Hormones and Behavior. 145: 105245. doi:10.1016/j.yhbeh.2022.105245. ISSN 0018-506X. PMID 35988450.
  132. ^ Grebe, Nicholas M.; Sheikh, Alizeh; Drea, Christine M. (2022-03-01). "Integrating the female masculinization and challenge hypotheses: Female dominance, male deference, and seasonal hormone fluctuations in adult blue-eyed black lemurs (Eulemur flavifrons)". Hormones and Behavior. 139: 105108. doi:10.1016/j.yhbeh.2022.105108. ISSN 0018-506X. PMID 35033896.
  133. ^ Wingfield, John C.; Ramenofsky, Marilyn; Hegner, Robert E.; Ball, Gregory F. (2020-07-01). "Whither the challenge hypothesis?". Hormones and Behavior. 30th Anniversary of the Challenge Hypothesis. 123: 104588. doi:10.1016/j.yhbeh.2019.104588. ISSN 0018-506X. PMID 31525343.
  134. ^ Phoenix, Charles H. (2009-05-01). "Organizing action of prenatally administered testosterone propionate on the Tissues mediating mating behavior in the female guinea pig". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 566. doi:10.1016/j.yhbeh.2009.01.004. ISSN 0018-506X. PMID 19302826.
  135. ^ Arnold, Arthur P. (2009-05-01). "The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 570–578. doi:10.1016/j.yhbeh.2009.03.011. ISSN 0018-506X. PMC 3671905. PMID 19446073.
  136. ^ Wallen, Kim (2009-05-01). "The Organizational Hypothesis: Reflections on the 50th anniversary of the publication of Phoenix, Goy, Gerall, and Young (1959)". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 561–565. doi:10.1016/j.yhbeh.2009.03.009. ISSN 0018-506X. PMID 19446072.
  137. ^ Hines, Melissa (2006-11-01). "Prenatal testosterone and gender-related behaviourThis paper was presented at the 4th Ferring Pharmaceuticals International Paediatric Endocrinology Symposium, Paris (2006). Ferring Pharmaceuticals has supported the publication of these proceedings". European Journal of Endocrinology. 155 (Supplement_1): S115 – S121. doi:10.1530/eje.1.02236. ISSN 0804-4643. PMID 17074984.
  138. ^ Arnold, Arthur P. (2009-05-01). "The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 570–578. doi:10.1016/j.yhbeh.2009.03.011. ISSN 0018-506X. PMC 3671905. PMID 19446073.
  139. ^ Arnold, Arthur P. (2020-04-01). "Sexual differentiation of brain and other tissues: Five questions for the next 50 years". Hormones and Behavior. 120: 104691. doi:10.1016/j.yhbeh.2020.104691. ISSN 0018-506X. PMC 7440839. PMID 31991182.
  140. ^ Krebs-Kraft, Desiree L.; McCarthy, Margaret M. (2011-01-01), Norris, David O.; Lopez, Kristin H. (eds.), "Chapter 1 - Sexual Differentiation of the Mammalian Brain", Hormones and Reproduction of Vertebrates, London: Academic Press, pp. 1–24, doi:10.1016/b978-0-12-374928-4.10001-x, ISBN 978-0-12-374928-4, retrieved 2025-01-02
  141. ^ Diamond, Milton (2009-05-01). "Clinical implications of the organizational and activational effects of hormones". Hormones and Behavior. 50th Anniversary of the Publication of Phoenix, Goy, Gerall & Young 1959: Organizational Effects of Hormones. 55 (5): 621–632. doi:10.1016/j.yhbeh.2009.03.007. ISSN 0018-506X. PMID 19446079.
  142. ^ Swaab, Dick F. (2007-09-01). "Sexual differentiation of the brain and behavior". Best Practice & Research Clinical Endocrinology & Metabolism. Normal and Abnormal Sex Development. 21 (3): 431–444. doi:10.1016/j.beem.2007.04.003. ISSN 1521-690X. PMID 17875490.
  143. ^ Makieva, Sofia; Saunders, Philippa T.K.; Norman, Jane E. (2014-07-01). "Androgens in pregnancy: roles in parturition". Human Reproduction Update. 20 (4): 542–559. doi:10.1093/humupd/dmu008. ISSN 1355-4786. PMC 4063701. PMID 24643344.
  144. ^ Parsons, Agata M.; Bouma, Gerrit J. (2021-07-01). "A Potential Role and Contribution of Androgens in Placental Development and Pregnancy". Life (Basel, Switzerland). 11 (7): 644. Bibcode:2021Life...11..644P. doi:10.3390/life11070644. ISSN 2075-1729. PMC 8305703. PMID 34357016.
  145. ^ Abruzzese, Giselle Adriana; Ferreira, Silvana Rocio; Ferrer, Maria José; Silva, Aimé Florencia; Motta, Alicia Beatriz (2023-01-01). "Prenatal Androgen Excess Induces Multigenerational Effects on Female and Male Descendants". Clinical Medicine Insights: Endocrinology and Diabetes. 16: 11795514231196461. doi:10.1177/11795514231196461. ISSN 1179-5514. PMC 10496475. PMID 37705939.
  146. ^ Wang, Yuqi; Riedstra, Bernd; Hulst, Ronja; Noordhuis, Roy; Groothuis, Ton (2023-03-01). "Early conversion of maternal androgens affects the embryo already in the first week of development". Biology Letters. 19 (3): 20220593. doi:10.1098/rsbl.2022.0593. PMC 9975654. PMID 36855858.
  147. ^ Udry, J. Richard; Morris, Naomi M.; Kovenock, Judith (1995-07-01). "Androgen effects on women's gendered behaviour". Journal of Biosocial Science. 27 (3): 359–368. doi:10.1017/S0021932000022884. ISSN 1469-7599. PMID 7650053.
  148. ^ Dloniak, S. M.; French, J. A.; Holekamp, K. E. (2006-04-27). "Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas". Nature. 440 (7088): 1190–1193. Bibcode:2006Natur.440.1190D. doi:10.1038/nature04540. ISSN 1476-4687. PMID 16641996.
  149. ^ Goymann, Wolfgang; East, Marion L.; Hofer, Heribert (2001-02-01). "Androgens and the Role of Female "Hyperaggressiveness" in Spotted Hyenas (Crocuta crocuta)". Hormones and Behavior. 39 (1): 83–92. doi:10.1006/hbeh.2000.1634. ISSN 0018-506X. PMID 11161886.
  150. ^ Ruuskanen, Suvi (2015-12-01). "Hormonally-mediated maternal effects in birds: Lessons from the flycatcher model system". General and Comparative Endocrinology. 224: 283–293. doi:10.1016/j.ygcen.2015.09.016. ISSN 0016-6480. PMID 26393309.
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