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"Paternal Behavior."
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The genetic basis of parental care evolution in monogamous mice
Parental care is essential for the survival of mammals, yet the mechanisms underlying its evolution remain largely unknown. Here we show that two sister species of mice,
Peromyscus polionotus
and
Peromyscus maniculatus
, have large and heritable differences in parental behaviour. Using quantitative genetics, we identify 12 genomic regions that affect parental care, 8 of which have sex-specific effects, suggesting that parental care can evolve independently in males and females. Furthermore, some regions affect parental care broadly, whereas others affect specific behaviours, such as nest building. Of the genes linked to differences in nest-building behaviour, vasopressin is differentially expressed in the hypothalamus of the two species, with increased levels associated with less nest building. Using pharmacology in
Peromyscus
and chemogenetics in
Mus
, we show that vasopressin inhibits nest building but not other parental behaviours. Together, our results indicate that variation in an ancient neuropeptide contributes to interspecific differences in parental care.
Parental care in mice evolves through multiple genetic changes; one candidate is vasopressin, the reduced expression of which promotes parental nest-building behaviour in monogamous mice.
Genetics of parental care
Rodents display a wide range of parental care behaviours, such as nest building, with some species more driven to perform these duties than others. However, the genetic and evolutionary mechanisms that influence the extent to which parental care behaviours are performed have remained unknown. Here, Hopi Hoekstra and colleagues utilize a quantitative genetic approach to identify genetic candidates that influence parental care in closely related mouse species. Genetic changes that enhance the levels of the hypothalamic hormone vasopressin were linked to less nest building. In addition, artificial manipulation of neurons releasing vasopressin could directly affect the extent of nest building, with lower vasopressin-releasing neuronal activity correlated with increased levels of nest building. This suggests that variation in neuropeptide signalling may contribute to complex social behaviours such as parental care.
Journal Article
A father's love
Throughout the animal kingdom and within snug houses, fathers express love for their children in their own unique ways. Includes facts about the animals featured.
Book
Functional circuit architecture underlying parental behaviour
Parenting is essential for the survival and wellbeing of mammalian offspring. However, we lack a circuit-level understanding of how distinct components of this behaviour are coordinated. Here we investigate how galanin-expressing neurons in the medial preoptic area (MPOA
Gal
) of the hypothalamus coordinate motor, motivational, hormonal and social aspects of parenting in mice. These neurons integrate inputs from a large number of brain areas and the activation of these inputs depends on the animal’s sex and reproductive state. Subsets of MPOA
Gal
neurons form discrete pools that are defined by their projection sites. While the MPOA
Gal
population is active during all episodes of parental behaviour, individual pools are tuned to characteristic aspects of parenting. Optogenetic manipulation of MPOA
Gal
projections mirrors this specificity, affecting discrete parenting components. This functional organization, reminiscent of the control of motor sequences by pools of spinal cord neurons, provides a new model for how discrete elements of a social behaviour are generated at the circuit level.
Galanin-expressing neurons in the medial preoptic area coordinate different aspects of motor, motivational, hormonal and social behaviour associated with parenting by projecting to different brain regions depending on the type of behaviour and sex and reproductive state of mice.
Journal Article
Neural control of maternal and paternal behaviors
Parental care, including feeding and protection of young, is essential for the survival as well as mental and physical well-being of the offspring. A large variety of parental behaviors has been described across species and sexes, raising fascinating questions about how animals identify the young and how brain circuits drive and modulate parental displays in males and females. Recent studies have begun to uncover a striking antagonistic interplay between brain systems underlying parental care and infant-directed aggression in both males and females, as well as a large range of intrinsic and environmentally driven neural modulation and plasticity. Improved understanding of the neural control of parental interactions in animals should provide novel insights into the complex issue of human parental care in both health and disease.
Journal Article
The neural mechanisms and consequences of paternal caregiving
In recent decades, human sociocultural changes have increased the numbers of fathers that are involved in direct caregiving in Western societies. This trend has led to a resurgence of interest in understanding the mechanisms and effects of paternal care. Across the animal kingdom, paternal caregiving has been found to be a highly malleable phenomenon, presenting with great variability among and within species. The emergence of paternal behaviour in a male animal has been shown to be accompanied by substantial neural plasticity and to be shaped by previous and current caregiving experiences, maternal and infant stimuli and ecological conditions. Recent research has allowed us to gain a better understanding of the neural basis of mammalian paternal care, the genomic and circuit-level mechanisms underlying paternal behaviour and the ways in which the subcortical structures that support maternal caregiving have evolved into a global network of parental care. In addition, the behavioural, neural and molecular consequences of paternal caregiving for offspring are becoming increasingly apparent. Future cross-species research on the effects of absence of the father and the transmission of paternal influences across generations may allow research on the neuroscience of fatherhood to impact society at large in a number of important ways.Recent years have seen a growing interest in the neurobiological basis of paternal caregiving. Feldman and colleagues review studies that have shed light on the circuits that underlie paternal care in mammals and the consequences of this care for fathers and their offspring.
Journal Article
Development of the paternal brain in expectant fathers during early pregnancy
The human parenting brain network mediates caregiving behaviors. When exposed to the stimuli of their infants, compared with non-parents, both fathers and mothers exhibit distinct patterns of neural activation. As human males, relative to females, do not undergo robust physiological changes during pregnancy, when and how the paternal brain networks begin to form remains unclear. Thus, using functional MRI, we examined brain activation in response to infant-interaction videos in two groups, childless males and first-time expectant fathers during their partners’ early pregnancy before remarkable changes in their partners’ appearances commenced. Multivoxel pattern analysis revealed that expectant fathers’ left anterior insula and inferior frontal gyrus showed incipient changes in response to parenthood during early pregnancy. Furthermore, these changes were associated with several paternal traits, such as a negative image toward parenting. Such external factors might influence the paternal brain's development during early pregnancy.
Journal Article
Pregnancy Risk Assessment Monitoring System for Dads: A piloted randomized trial of public health surveillance of recent fathers’ behaviors before and after infant birth
Becoming a father impacts men's health and wellbeing, while also contributing to the health and wellbeing of mothers and children. There is no large-scale, public health surveillance system aimed at understanding the health and behaviors of men transitioning into fatherhood. The purpose of this study was to describe piloted randomized approaches of a state-based surveillance system examining paternal behaviors before and after their infant's birth to better understand the health needs of men and their families during the transition to parenthood.
During October 2018-July 2019, 857 fathers in Georgia were sampled 2-6 months after their infant's birth from birth certificates files and surveyed via mail, online or telephone, in English or Spanish, using two randomized approaches: Indirect-to-Dads and Direct-to-Dads. Survey topics included mental and physical health, healthcare, substance use, and contraceptive use.
Weighted response rates (Indirect-to-Dads, 33%; Direct-to-Dads, 31%) and population demographics did not differ by approach. Respondents completed the survey by mail (58%), online (28%) or telephone (14%). Among 266 fathers completing the survey, 55% had a primary care physician, and 49% attended a healthcare visit for themselves during their infant's mother's pregnancy or since their infant's birth. Most fathers were overweight or had obesity (70%) while fewer reported smoking cigarettes (19%), binge drinking (13%) or depressive symptoms (10%) since their infant's birth.
This study tests a novel approach for obtaining population-based estimates of fathers' perinatal health behaviors, with comparable response rates from two pragmatic approaches. The pilot study results quantify a number of public health needs related to fathers' health and healthcare access.
Journal Article
Vasopressin-to-oxytocin receptor crosstalk in the preoptic area underlying parental behaviors in male mice
The transition to parenthood brings significant changes in behavior toward offspring. For instance, in anticipation of their offspring, male mice shift from infanticidal to caregiving behaviors. While the release of oxytocin from the paraventricular hypothalamus (PVH) plays a critical role in paternal caregiving, it does not fully account for the entire behavioral shift. The specific downstream neurons and signaling mechanisms involved in this process remain obscure. Here, we demonstrate that PVH vasopressin neurons also essentially contribute to a paternal behavioral shift. This vasopressin signal is partially transmitted through oxytocin receptors (OTRs) expressed in the anterior commissure and medial nuclei of the preoptic area. These OTR-expressing neurons receive inputs from both PVH oxytocin and vasopressin neurons and are responsible for expressing paternal caregiving behaviors. Collectively, this non-canonical vasopressin-to-OTR crosstalk within specific limbic circuits acts as a pivotal regulator of paternal behavioral changes in mice.
Neural mechanisms underlying shift toward caregiving behaviors in male animals are not fully understood. Here authors show that parental behaviors in male mice are facilitated by vasopressin released from the hypothalamus. Downstream, oxytocin receptors expressed in the preoptic area mediate this effect via noncanonical ligand–receptor crosstalk.
Journal Article
Monoamine neurochemistry, behavior, and microhabitat contribute to male coquí frog modes: silent, territorial, and paternal
Monoaminergic neurotransmitters are essential for a multitude of physiological and behavioral functions including territoriality and parental care. The Puerto Rican coquí frog,
Eleutherodactylus coqui
, possesses an intriguing multi-modal male behavioral organization whereby males can be territorial, paternal, and silent (non-calling). The objective of this study was to quantify central monoamines in the three male modes and integrate this neurochemistry with data from microhabitat shelter selection and male social structure. Males were assessed for monoamines and metabolites using high performance liquid chromatography with electrochemical detection. Results indicated that there are distinct and significant differences among the three male behavioral modes based on male social structure, microhabitat shelter selection, and neurochemistry. Silent males are non-combative, quiescent, occur nocturnally in relatively open locations with sparser vegetation, and are characterized by high levels of epinephrine and norepinephrine in several forebrain nuclei. Territorial males emit vocalizations, are typically surrounded by more vegetation than silent males, may have a silent male within their territory, and are denoted by significantly higher levels of norepinephrine in the preoptic area and ventral hypothalamus and dopamine in the amygdala responsible male territorial behaviors. Paternal males brood and guard developing embryos in secluded nest sites that are surrounded by vegetation, not within territories of residential males, and typically not in close proximity of silent males. Paternal brains have significantly higher levels epinephrine and serotonin in the raphe and reticular nuclei indicating the necessity to regulate metabolic processes and stress during the period of prolong paternal care.
Journal Article