Alloparental Behavior and Paternal Behavior in Nonhuman Mammals

Chapter 7 examines alloparental and paternal behavior. Although these behaviors are rare in mammals, their occurrence indicates that parental behavior can occur in the absence of pregnancy and parturition. For mammals of both sexes, dual brain circuits affect whether parental behavior occurs: An inhibitory defensive circuit (anterior hypothalamus/ventromedial hypothalamus projections to periaqueductal gray), and an excitatory parental circuit (medial preoptic area, mesolimbic dopamine system, and the oxytocin system). When alloparental behavior occurs, either through experimental genetic selection (virgin female laboratory house mice) or through natural selection (prairie voles, marmosets), the defensive circuit has been downregulated and the parental circuit has been upregulated by such selection. When paternal behavior occurs, either naturally (California mice, dwarf hamsters) or experimentally (laboratory rats and house mice), copulation with a female and remaining with her through parturition depresses the male’s defensive circuitry while activating his parental circuitry.

Parental Behavior

Chapter 2 describes the types of parental behavior that can occur in vertebrates: maternal, paternal, and alloparental behavior. The dominant form of parental behavior in mammals is a uniparental maternal care system, where the mother raises her offspring by herself. A mother can form either a nonselective or selective bond with her infants, depending on the maturity of her infants at birth. A biparental care system, in which both maternal and paternal behavior occur, is present in about 5% of mammalian species. Approximately 3% of mammalian species exhibit a cooperative breeding system, where some offspring remain in their social group and help their parents raise subsequent offspring. The parental behavior of these helpers is referred to as alloparental behavior. The occurrence of paternal and alloparental behavior shows that alternative mechanisms, not requiring pregnancy and parturition, can evolve which allow for these forms of parental behavior.

Evolutionary Perspectives on the Parental Brain

Chapter 11 presents evolutionary perspectives on the parental brain. First, the evolution of neural modifications to the parental brain that may have allowed for the emergence of alloparental behavior is re-examined. Second, evidence is presented for the proposal that the parental brain provided the foundation or template for the evolution of other types of strong prosocial bonds in mammals, such as the pair bond that occurs in biparental monogamous species, and the hyper-cooperation and hyper-prosociality directed toward in-group members, as opposed to out-group members, that occur in human societies. With respect to the latter, neural mechanisms associated with alloparenting and cooperative breeding may have served as a preadaptation. Neural models, along with evidence, are presented to show how cortical and subcortical parental brain circuits may have been appropriated and utilized by natural selection to result in the evolution of high levels of prosociality within human social groups.

The Parental Brain

The Parental Brain: Mechanisms, Development, and Evolution takes a three-pronged approach to the parental brain. The first part of the book deals with neural mechanisms. Subcortical circuits are crucially involved in parental behavior, and, for most mammals, the physiological events of pregnancy and parturition prime these circuits so that they become responsive to infant stimuli, allowing for the onset of maternal behavior at parturition. However, since paternal behavior and alloparental behavior occur in some mammalian species, alternate mechanisms are shown to exist that regulate the access of infant stimuli to these circuits. In humans, cortical circuits interact with subcortical circuits so that parental feeling states (emotions) and cognitions can be translated into parental behavior. The section on development emphasizes the experiential basis of the intergenerational continuity of normal and abnormal maternal behavior in animals and humans: The way a mother treats her infant affects the development of the infant’s brain and subsequent maternal behavior. Genetic factors, including epigenetic processes and gene by environment (G × E) interactions, are also involved. The chapter on evolution presents evidence that the parental brain most likely provided the foundation or template for other strong prosocial bonds. In particular, cortical and subcortical parental brain circuits have probably been utilized by natural selection to promote the evolution of the hyper-cooperation and hyper-prosociality that exist in human social groups. A unique aspect of this book is its integration of animal and human research to create a complete understanding of the parental brain.

Hormonal Control of Maternal Behavior in Nonhuman Mammals

Chapter 3 describes the hormones that promote the immediate onset of maternal behavior at parturition, drawing on research from rats, rabbits, sheep, mice, and nonhuman primates. The critical hormones include rising levels of estradiol, prolactin, and placental lactogens that occur near the end of pregnancy on a background of progesterone withdrawal. In contrast to the onset of maternal behavior, due to maternal experience, its maintenance does not require hormones. Laboratory strains of female mice, produced by inbreeding and selective breeding, are anomalous in that they do not require pregnancy hormones to show prompt maternal behavior when presented with conspecific infants under low-stress conditions. However, the physiological events of late pregnancy boost maternal motivation in these mice to allow for effective maternal behavior in challenging environments. The same processes operate in species that exhibit naturally occurring alloparental behavior, such as marmosets, where such behavior has evolved by natural selection.

Forgotten, But Not Lost—Alloparental Behavior and Pup–Adult Interactions in Companion Dogs

Socialization with humans is known to be a pivotal factor in the development of appropriate adult dog behavior, but the role and extent of dog–dog interactions in the first two months of life is rarely studied. Although various forms of alloparental behaviors are described in the case of wild-living canids, the social network of companion dogs around home-raised puppies is almost unknown. An international online survey of companion dog breeders was conducted, asking about the interactions of other dogs in the household with the puppies and the pups’ mother. Based on the observations of these breeders, our study showed an intricate network of interactions among adult dogs and puppies below the age of weaning. Alloparental behaviors (including suckling and feeding by regurgitation) were reportedly common. Independent of their sex, other household dogs mostly behaved in an amicable way with the puppies, and in the case of unseparated housing, the puppies reacted with lower fear to the barks of the others. Parousness, sexual status, and age of the adult dogs had an association with how interested the dogs were in interacting with the puppies, and also with how the mother reacted to the other dogs. Our study highlights the possible importance of dog–dog interactions during the early life of puppies in forming stable and low-stress interactions with other dogs later in life.