Fathering in rodents: Neurobiological substrates and consequences for offspring

This article is part of a Special Issue “Parental Care”. Paternal care, though rare among mammals, is routinely displayed by several species of rodents. Here we review the neuroanatomical and hormonal bases of paternal behavior, as well as the behavioral and neuroendocrine consequences of paternal behavior for offspring. Fathering behavior is subserved by many of the same neural substrates which are also involved in maternal behavior (for example, the medial preoptic area of the hypothalamus). While gonadal hormones such as testosterone, estrogen, and progesterone, as well as hypothalamic neuropeptides such as oxytocin and vasopressin, and the pituitary hormone prolactin, are implicated in the activation of paternal behavior, there are significant gaps in our knowledge of their actions, as well as pronounced differences between species. Removal of the father in biparental species has long-lasting effects on behavior, as well as on these same neuroendocrine systems, in offspring. Finally, individual differences in paternal behavior can have similarly long-lasting, if more subtle, effects on offspring behavior. Future studies should examine similar outcome measures in multiple species, including both biparental species and closely related uniparental species. Careful phylogenetic analyses of the neuroendocrine systems presumably important to male parenting, as well as their patterns of gene expression, will also be important in establishing the next generation of hypotheses regarding the regulation of male parenting behavior.     

Top-down approaches to the study of natural variation in complex physiological pathways using the white-footed mouse (Peromyscus leucopus) as a model

Variation in complex physiological pathways has important effects on human function and medical treatment. Complex pathways involve cells at multiple locations, which serve different functions regulated by many genes and include complex neuroendocrine pathways that regulate physiological function. One of two competing hypotheses regarding the effects of selection on complex pathways predicts that variability should be common within complex pathways. If this hypothesis is correct, then we should expect wide variation in neuroendocrine function to be typical within natural populations. To test this hypothesis, a complex neuroendocrine pathway that regulates photoperiod-dependent changes in fertility in a natural population of white-footed mice (Peromyscus leucopus) was used to test for natural genetic variability in multiple components of the pathway. After testing only six elements in the photoperiod pathway in P. leucopus, genetic variation in the following four of these elements was evident: the circadian clock, melatonin receptor abundance or affinity, sensitivity of the reproductive axis to steroid negative feedback, and gonadotropin-releasing hormone neuronal activity. If this result can be extended to humans, the prediction would be that significant variation at multiple loci in complex neuroendocrine pathways is common among humans, and that variation would exist even in human populations from a common genetic background. This finding could only be drawn from an "exotic" animal model derived from a natural source population, confirming the continuing importance of nontraditional models alongside the standard laboratory species.     

Application of organization-activation theory to alternative male reproductive strategies: a review

Many species have extreme within-sex morphological and behavioral polymorphisms, most commonly different male phenotypes that practice different reproductive strategies. Although much is known about the role of hormones in sexual differentiation, little is known about what role hormones might play in within-sex differentiation. The relative plasticity hypothesis is derived from the classical organization-activation model of hormone action. It distinguishes between two types of polymorphic systems: a fixed system in which individual males assume one phenotype for their adult lives and a plastic system in which individual males can change phenotypes at least once. By analogy to sexual differentiation, the relative plasticity hypothesis generally predicts that organizational influences of hormones will be more important in fixed systems and activational influences of hormones will be more important in plastic systems. A review of our knowledge of the role of hormones in differentiation of within-sex polymorphisms indicates that the relative plasticity hypothesis accounts for otherwise diverse and contradictory results. This further supports the hypothesis that the organizational-activational model of hormone action derived from sexual differentiation generalizes to within-sex polymorphisms. However, studies of the effects of hormone manipulations on within-sex differentiation are rare but are desperately needed to further our understanding of this problem. Further studies of discontinuous behavioral variation characteristic of polymorphic species may further our understanding of the physiological basis of within-sex behavior variation in all species.     

动物个性研究进展

"个性"是指不同时空条件下动物种群个体间行为的稳定差异。大量的理论和实验性研究表明,个性差异在动物界普遍存在,其是种群多度和分布、物种共存及群落构建的重要驱动因子。介绍了动物个性的概念、分类及衡量指标,将前人测量个性类型的方法加以总结;随后介绍了动物个性的生态学意义,尤其是个性对动物生活史策略、种群分布与多度、群落结构和动态、生态系统功能和过程以及疾病与信息传播等的影响。在此基础上,进一步分析了在人类活动增加等全球变化背景下,动物个性如何调控动物个体行为、种群和群落动态对这些环境变化的响应。阐述了动物个性的形成与维持机制,并对未来的研究方向进行了展望。     

Maternal imprints and the origins of variation

The non-genomic transmission of maternal behavior from one generation to the next illustrates the pervasive influence of maternal care on offspring development and the high degree of plasticity within the developing maternal brain. Investigations of the mechanisms through which these maternal effects are achieved have demonstrated environmentally-induced changes in gene expression associated with epigenetic modifications within the promoter region of target genes. These findings raise challenging questions regarding the pathways linking experience to behavioral variation and the broader ecological/evolutionary implications of the dynamic changes in neuroendocrine function that emerge. This review will highlight studies in laboratory rodents which demonstrate plasticity in the maternal brain and the role of maternally-induced changes in DNA methylation in establishing the link between variations in maternal care and consequent developmental outcomes. The persistence of maternal effects across generations and the trade-offs in reproduction that are evident in female offspring who experience high vs. low levels of maternal care contribute to our understanding of the divergent strategies that are triggered by the quality of early-life experiences. Evolving concepts of inheritance and the interplay between genes and the environment may advance our understanding of the origins of individual differences in phenotype.     

Towards an integrative model of sociality in caviomorph rodents

In the late 1990s and early 2000s it was recognized that behavioral ecologists needed to study the sociality of caviomorph rodents (New World hystricognaths) before generalizations about rodent sociality could be made. Researchers identified specific problems facing individuals interested in caviomorph sociality, including a lack of information on the proximate mechanisms of sociality, role of social environment in development, and geographical or intraspecific variation in social systems. Since then researchers have described the social systems of many previously understudied species, including some with broad geographical ranges. Researchers have done a good job of determining the role of social environments in development and identifying the costs and benefits of social living. However, relatively little is known about the proximate mechanisms of social behavior and fitness consequences, limiting progress toward the development of integrative (evolutionary-mechanistic) models for sociality. To develop integrative models behavioral ecologists studying caviomorph rodents must generate information on the fitness consequences of different types of social organization, brain mechanisms, and endocrine substrates of sociality. We review our current understanding and future directions for research in these conceptual areas. A greater understanding of disease ecology, particularly in species carrying Old World parasites, is needed before we can identify potential links between social phenotypes, mechanism, and fitness.     

Neurobiology of sexual behavior

Recent advances in the neurobiology of sexual behavior have helped to refine our understanding of the neuroanatomical, neuroendocrine and neurochemical systems that modulate responses to sexual stimulation. Both appetitive and consummatory sexual behaviors have been studied in several laboratory species and in humans using traditional and novel behavioral paradigms. New knowledge has emerged concerning the role of hypothalamic, limbic and brainstem structures, neuropeptides, brain monoamines and nitric oxide in the control of partner preference, sexual desire, erection, copulation, ejaculation, orgasm and sexual satiety. Brain imaging of visually evoked sexual arousal in humans has also been examined.     

To subjugate NPY is to improve the quality of life and live longer

The interactive network of neuropeptide Y (NPY) and cohorts is necessary for integrating the hypothalamic regulation of appetite and energy expenditure with the endocrine and neuroendocrine systems on a daily basis. Genetic and environmental factors that produce an insufficiency of leptin restraint on NPY and cognate receptors deregulate the homeostasis to engender various life-threatening risk factors. Recent studies from our laboratory show that neurotherapy consisting of a single central administration of recombinant adeno-associated virus vector encoding the leptin gene can repress the hypothalamic NPY system for the lifetime of rodents. A major benefit of this stable tonic restraint is deceleration of pathophysiologic sequalae that shorten life span. These include suppression of weight gain, fat accumulation, circulating adipokines, amelioration of major symptoms of metabolic syndrome, improved reproduction and bone health. Thus, sustained repression of NPY signaling in the hypothalamus by leptin transgene expression can improve the quality of life and extend longevity.     

Macro- and micro-habitat selection of small rodents and their predation risk perception under a novel invasive predator at the southern end of the Americas

Invasive predators are responsible for the extinction of numerous island species worldwide. The naïve prey hypothesis suggests that the lack of co-evolutionary history between native prey and introduced predators results in the absence of behavioral responses to avoid predation. The lack of terrestrial mammal predators is a core feature of islands at the southern end of the Americas. Recently, however, the American mink (Neovison vison) established as a novel terrestrial predator, where rodents became a main portion of its diet. Here, we investigated on Navarino Island, Chile, macro- and micro-habitat selection of small rodents using Sherman traps. Additionally, we experimentally tested behavioral responses of small rodents to indirect cues of native raptorial predation risk (vegetation cover) and direct cues of novel mink predation risk (gland odor) using Sherman traps and foraging trays (giving-up density (GUD)). At the macro-habitat level, we detected native rodents of the species Abrothrix xanthorhinus and Oligoryzomys longicaudatus and the exotic Mus musculus. In general, rodents preferred scrubland habitats. At the micro-habitat level, we only captured individuals of A. xanthorhinus. They preferred covered habitats with tall vegetation. GUD increased in opened areas (riskier for raptorial predation) regardless of the presence or not of mink odor. These results suggest that A. xanthorhinus can perceive predation risk by raptors, but not by mink, results that accord with the hypothesis that co-evolutionary history is important for rodents to develop antipredator behavior. Given that these rodents represent an important proportion of mink diet, the low abundances together with the apparent lack of antipredator response raise conservation concerns for the small rodent populations inhabiting the southernmost island ecosystems of the Americas.     

Estrous behavior in dairy cows: identification of underlying mechanisms and gene functions

Selection in dairy cattle for a higher milk yield has coincided with declined fertility. One of the factors is reduced expression of estrous behavior. Changes in systems that regulate the estrous behavior could be manifested by altered gene expression. This literature review describes the current knowledge on mechanisms and genes involved in the regulation of estrous behavior. The endocrinological regulation of the estrous cycle in dairy cows is well described. Estradiol (E2) is assumed to be the key regulator that synchronizes endocrine and behavioral events. Other pivotal hormones are, for example, progesterone, gonadotropin releasing hormone and insulin-like growth factor-1. Interactions between the latter and E2 may play a role in the unfavorable effects of milk yield-related metabolic stress on fertility in high milk-producing dairy cows. However, a clear understanding of how endocrine mechanisms are tied to estrous behavior in cows is only starting to emerge. Recent studies on gene expression and signaling pathways in rodents and other animals contribute to our understanding of genes and mechanisms involved in estrous behavior. Studies in rodents, for example, show that estrogen-induced gene expression in specific brain areas such as the hypothalamus play an important role. Through these estrogen-induced gene expressions, E2 alters the functioning of neuronal networks that underlie estrous behavior, by affecting dendritic connections between cells, receptor populations and neurotransmitter releases. To improve the understanding of complex biological networks, like estrus regulation, and to deal with the increasing amount of genomic information that becomes available, mathematical models can be helpful. Systems biology combines physiological and genomic data with mathematical modeling. Possible applications of systems biology approaches in the field of female fertility and estrous behavior are discussed.     

Short days and exogenous melatonin increase aggression of male Syrian hamsters (Mesocricetus auratus)

Many nontropical rodent species rely on photoperiod as a primary cue to coordinate seasonally appropriate changes in physiology and behavior. Among these changes, some species of rodents demonstrate increased aggression in short, "winter-like" compared with long "summer-like" day lengths. The precise neuroendocrine mechanisms mediating changes in aggression, however, remain largely unknown. The goal of the present study was to examine the effects of photoperiod and exogenous melatonin on resident-intruder aggression in male Syrian hamsters (Mesocricetus auratus). In Experiment 1, male Syrian hamsters were housed in long (LD 14:10) or short (LD 10:14) days for 10 weeks. In Experiment 2, hamsters were housed in long days and half of the animals were given daily subcutaneous melatonin injections (15 microg/day in 0.1 ml saline) 2 h before lights out for 10 consecutive days to simulate a short-day pattern of melatonin secretion, while the remaining animals received injections of the vehicle alone. Animals in both experiments were then tested using a resident-intruder model of aggression and the number of attacks, duration of attacks, and latency to initial attack were recorded. In Experiment 1, short-day hamsters underwent gonadal regression and displayed increased aggression compared with long-day animals. In Experiment 2, melatonin treatment also increased aggression compared with control hamsters without affecting circulating testosterone. Collectively, the results of the present study demonstrate that exposure to short days or short day-like patterns of melatonin increase aggression in male Syrian hamsters. In addition, these results suggest that photoperiodic changes in aggression provide an important, ecologically relevant model with which to study the neuroendocrine mechanisms underlying aggression in rodents.     

Steroid imprinting and modulation of sexual dimorphism in the luteinizing hormone-releasing hormone neuronal system

Summary 1. Sex differences in the control of gonadotropin secretion and reproductive functions are a distinct characteristic in all mammalian species, including humans. Ovulation and cyclicity are among the most distinct neuroendocrine markers of female brain differentiation, along with sex behavioral traits that are also evident in different species.2. The luteinizing hormone-releasing hormone (LHRH) neuronal system is the prime regulator of neuroendocrine events leading to ovulation and hormonal changes during the menstrual cycle and, as such, is the potential site where many of these sex differences may be expressed or, at the very least, integrated. However, until recently, no significant differences were seen in LHRH neurons between male and female brains, including cell number, pattern of distribution, and expression of message or peptide (LHRH) levels.3. Recently, we reported that galanin (GAL), a brain-gut peptide, is coexpressed in LHRH neurons and that this coexpression is sexually dimorphic. When GAL is used as a marker for this neuronal system, it is clear that estradiol as well as progesterone profoundly affects the message and expression of the peptide and that this regulation, at least in rodents, is neonatally predetermined by gonadal steroid imprinting.4. Changes in GAL expression and message can also be seen at puberty, during pregnancy and lactation, and in aging, all situations that affect the function of the LHRH neuronal system. Using an immortalized LHRH neuronal cell line (GT1) we have recently observed that these neurons express estrogen receptor (ER) and GAL and that estradiol can increase the expression of GAL, indicating functional activation of the endogenous ER.     

Neuroendocrine and behavioral implications of endocrine disrupting chemicals in quail

Studies in our laboratory have focused on endocrine, neuroendocrine, and behavioral components of reproduction in the Japanese quail. These studies considered various stages in the life cycle, including embryonic development, sexual maturation, adult reproductive function, and aging. A major focus of our research has been the role of neuroendocrine systems that appear to synchronize both endocrine and behavioral responses. These studies provide the basis for our more recent research on the impact of endocrine disrupting chemicals (EDCs) on reproductive function in the Japanese quail. These endocrine active chemicals include pesticides, herbicides, industrial products, and plant phytoestrogens. Many of these chemicals appear to mimic vertebrate steroids, often by interacting with steroid receptors. However, most EDCs have relatively weak biological activity compared to native steroid hormones. Therefore, it becomes important to understand the mode and mechanism of action of classes of these chemicals and sensitive stages in the life history of various species. Precocial birds, such as the Japanese quail, are likely to be sensitive to EDC effects during embryonic development, because sexual differentiation occurs during this period. Accordingly, adult quail may be less impacted by EDC exposure. Because there are a great many data available on normal development and reproductive function in this species, the Japanese quail provides an excellent model for examining the effects of EDCs. Thus, we have begun studies using a Japanese quail model system to study the effects of EDCs on reproductive endocrine and behavioral responses. In this review, we have two goals: first, to provide a summary of reproductive development and sexual differentiation in intact Japanese quail embryos, including ontogenetic patterns in steroid hormones in the embryonic and maturing quail. Second, we discuss some recent data from experiments in our laboratory in which EDCs have been tested in Japanese quail. The Japanese quail provides an excellent avian model for testing EDCs because this species has well-characterized reproductive endocrine and behavioral responses. Considerable research has been conducted in quail in which the effects of embryonic steroid exposure have been studied relative to reproductive behavior. Moreover, developmental processes have been studied extensively and include investigations of the reproductive axis, thyroid system, and stress and immune responses. We have conducted a number of studies, which have considered long-term neuroendocrine consequences as well as behavioral responses to steroids. Some of these studies have specifically tested the effects of embryonic steroid exposure on later reproductive function in a multigenerational context. A multigenerational exposure provides a basis for understanding potential exposure scenarios in the field. In addition, potential routes of exposure to EDCs for avian species are being considered, as well as differential effects due to stage of the life cycle at exposure to an EDC. The studies in our laboratory have used both diet and egg injection as modes of exposure for Japanese quail. In this way, birds were exposed to a specific dose of an EDC at a selected stage in development by injection. Alternatively, dietary exposure appears to be a primary route of exposure; therefore experimental exposure through the diet mimics potential field situations. Thus, experiments should consider a number of aspects of exposure when attempting to replicate field exposures to EDCs.     

Recent advances in behavioral neuroendocrinology: insights from studies on birds

Ever since investigations in the field of behavioral endocrinology were hatched with experiments on roosters, birds have provided original insights into issues of fundamental importance for all vertebrate groups. Here we focus on more recent advances that continue this tradition, including (1) environmental regulation of neuroendocrine and behavioral systems, (2) steroidogenic enzyme functions that are related to intracrine processes and de novo production of neurosteroids, and (3) hormonal regulation of neuroplasticity. We also review recent findings on the anatomical and functional organization of steroid-sensitive circuits in the basal forebrain and midbrain. A burgeoning body of data now demonstrates that these circuits comprise an evolutionarily conserved network, thus numerous novel insights obtained from birds can be used (in a relatively straightforward manner) to generate predictions for other taxa as well. We close by using birdsong as an example that links these areas together, thereby highlighting the exceptional opportunities that birds offer for integrative studies of behavioral neuroendocrinology and behavioral biology in general.     

The value of comparative approaches to our understanding of puberty as illustrated by investigations in birds and reptiles

This article is part of a Special Issue "Puberty and Adolescence". Studies of birds and reptiles have provided many basic insights into the neuroendocrine control of reproductive processes. This research has elucidated mechanisms regulating both early development, including sexual differentiation, and adult neuroendocrine function and behavior. However, phenomena associated with the transition into sexual maturation (puberty) have not been a focus of investigators working on species in these taxonomic classes. Research is complicated in birds and reptiles by a variety of factors, including what can be extended times to maturation, the need to reach particular body size regardless of age, and environmental conditions that can support or inhibit endocrine responses. However, careful selection of model systems, particularly those with available genetic tools, will lead to important comparative studies that can elucidate both generalizability and diversity of mechanisms regulating the onset of reproductive maturity.     

The head-fixed behaving rat—Procedures and pitfalls

This paper describes experimental techniques with head-fixed, operantly conditioned rodents that allow the control of stimulus presentation and tracking of motor output at hitherto unprecedented levels of spatio-temporal precision. Experimental procedures for the surgery and behavioral training are presented. We place particular emphasis on potential pitfalls using these procedures in order to assist investigators who intend to engage in this type of experiment. We argue that head-fixed rodent models, by allowing the combination of methodologies from molecular manipulations, intracellular electrophysiology, and imaging to behavioral measurements, will be instrumental in combining insights into the functional neuronal organization at different levels of observation. Provided viable behavioral methods are implemented, model systems based on rodents will be complementary to current primate models—the latter providing highest comparability with the human brain, while the former offer hugely advanced methodologies on the lower levels of organization, for example, genetic alterations, intracellular electrophysiology, and imaging.     

Managing genetic variation in tropical trees: linking knowledge with action in agroforestry ecosystems for improved conservation and enhanced livelihoods

Tree species in agroforestry ecosystems contribute to the livelihoods of rural communities and play an important role in the conservation of biodiversity. Unless agroforestry landscapes are productive, however, farmers will not maintain or enhance the range and quality of tree species in them, and both income opportunities and biodiversity will be lost. Productivity depends on both tree species diversity and genetic (intra-specific) variation, but research on the latter has until recently not received the recognition it deserves. Worse, when knowledge on tree genetic variation in agroforestry systems has become available, it has not generally been linked in any systematic way with management, indicating a disjunction between research and field-level practice. In this essay, we attempt to bridge this gap by considering three questions: why is genetic diversity important in tree species? What is our current state of knowledge about intra-specific variation in trees in agroforestry systems? And, finally, what practical interventions are possible to support the conservation of this diversity in agricultural landscapes, while enhancing farmers’ livelihoods? A wide genetic base in agroforestry trees is essential to prevent inbreeding depression and allow adaptation to changing environmental conditions and to altering markets for tree products. Recent evidence shows, however, that many species are subject to poor germplasm collection practice, occur at low densities in farmland, and are found in highly aggregated distributions, all of which observations raise concerns about productivity and sustainability. A range of germplasm-access based interventions is necessary to improve current management, including the enhancement of community seed- and seedling-exchange networks, and the development of locally based tree domestication activities. Equally necessary, but more difficult to address, is the development of markets that support genetic diversity in tropical tree species; we discuss approaches by which this may be undertaken.     

The head-fixed behaving rat--procedures and pitfalls

This paper describes experimental techniques with head-fixed, operantly conditioned rodents that allow the control of stimulus presentation and tracking of motor output at hitherto unprecedented levels of spatio-temporal precision. Experimental procedures for the surgery and behavioral training are presented. We place particular emphasis on potential pitfalls using these procedures in order to assist investigators who intend to engage in this type of experiment. We argue that head-fixed rodent models, by allowing the combination of methodologies from molecular manipulations, intracellular electrophysiology, and imaging to behavioral measurements, will be instrumental in combining insights into the functional neuronal organization at different levels of observation. Provided viable behavioral methods are implemented, model systems based on rodents will be complementary to current primate models--the latter providing highest comparability with the human brain, while the former offer hugely advanced methodologies on the lower levels of organization, for example, genetic alterations, intracellular electrophysiology, and imaging.     

Neuronal effects of orexins: relevant to sympathetic and cardiovascular functions

Orexin A and B, also called hypocretin 1 and 2, were recently discovered in the hypothalamus. This organ, in which a number of neuropeptides have been demonstrated to stimulate or suppress food intake, is considered important for the regulation of appetite and energy homeostasis. Orexins were initially reported as a regulator of food intake. More recent reports suggest their possible important roles in the multiple functions of neuronal systems, such as narcolepsy, a sleep disorder. Orexins and their receptors are distributed in neural tissue and brain regions involved in the autonomic and neuroendocrine control. Functional studies have shown that these peptides evoke changes in cardiovascular and sympathetic responses. The data from our in vivo and in vitro studies suggest that the peptide acting on neurons in the hypothalamic paraventricular nucleus increases the cardiovascular responses. This review will focus on the neural effects of orexins and how these peptides may participate in the regulation of cardiovascular and sympathetic functions.