Fathering in rodents: Neurobiological substrates and consequences for offspring

Abstract

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.

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation

“…Some of these changes differ across species, and their functional significance, including potential effects on paternal behavior, is generally unknown. Endocrine and neuroendocrine changes in fathers, as well as their possible functions, have been reviewed in detail recently (Saltzman and Ziegler 2014;Bales and Saltzman 2016). Therefore, we discuss them only briefly here, focusing primarily on experimental rather than correlational findings.…”

“…Paternal care is often associated with social monogamy and can involve such behaviors as warming, feeding, protecting, retrieving, and grooming infants, depending on the species (Kleiman and Malcolm 1981). In these biparental mammals, fathers can make important and lasting contributions to the survival and development of their offspring, including effects on social, reproductive and aggressive behavior, neural development, endocrine function, emotionality, and cognition that persist into adulthood (reviewed in Braun and Champagne 2014;Bales and Saltzman 2016).…”

Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior

“…Effects of hormones on behavior, and vice versa, can also differ among species and between the sexes, can change with age, and can vary among individuals with different experiential or genetic backgrounds (Pfaff et al 2004). Among biparental rodents, for example, testosterone inhibits the expression of paternal care by fathers in some species but enhances paternal care in others (Bales and Saltzman 2016). …”

Fatherhood alters gene expression within the MPOA

“…Therefore, the presence of the male, and particularly active participation of the male in fathering, is an unusual situation seen only in our own and a limited number of other mammalian species (4)(5)(6)(7)(8). In species where it does exist, including humans, paternal care is often crucial to the survivorship of offspring, or at the least has significant and longterm impacts on growth as well as neural, reproductive and social development (9,10). In biparental species, both mothers and fathers contribute to the care of offspring, however little is known about the specific neurobiological regulation of paternal care (6).…”

“…In biparental species, both mothers and fathers contribute to the care of offspring, however little is known about the specific neurobiological regulation of paternal care (6). The vast majority of parenting research focuses on the mother, while the role of the father is mostly considered in the context of paternal absence (9).…”