Animal Models of Paternal Behavior

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Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews
journal homepage: www.elsevier.com/locate/neubiorev

Review

Modeling Dad: Animal models of paternal behavior
Amanda C. Kentner a,*, Alfonso Abizaid b, Catherine Bielajew c
a

Hotckiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 4N1
Institute of Neuroscience, Carleton University, Ottawa, Ontario, Canada K1S 5B6
c
School of Psychology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5
b

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 10 June 2009
Received in revised form 31 August 2009
Accepted 31 August 2009

In humans, paternal behaviors have a strong influence on the emotional and social development of
children. Fathers, more frequently than mothers, leave the family nucleus, and/or become abusive,
leading to offspring that are more likely to grow under stressful conditions and greater susceptibility to
abnormal health and social outcomes. Literature on parental behaviors, human or animal, has primarily
focused on the interactions between mothers and offspring, with little research directed at
understanding paternal behavior. In animal studies, experimenters correlate paternal behaviors with
those seen in rodent or primate mothers, often under situations in which behaviors such as nest
protection, huddling, pup grooming, and retrieval are artificially induced. In humans, the majority of the
studies have looked at paralleling hormonal changes in fathers with those occurring in mothers, or
observed paternal behaviors in populations with specific anthropological backgrounds. These studies
reveal commonalities in parental behaviors and their underlying neural circuits. However, this work
highlights the possibility that paternal behavior has components that are strictly masculine with unique
neurobiological mechanisms. This review summarizes this information and provides a current view of a
topic that needs further exploration.
ß 2009 Elsevier Ltd. All rights reserved.

Keywords:
Paternal behavior
Maternal behavior
Animal model
Hormone
Neural basis
Sex differences
Parental investment
Social modeling
Polygamous
Monogamous

Contents
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Parental investment and parental behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Human parental systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Human paternal influence and offspring success . . . . . . . . . . . . . . . . . . . . . . . .
Paternal measurement issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Human paternal behavior and endocrine changes . . . . . . . . . . . . . . . . . . . . . . .
The model animal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Nest cleaning: measurement of paternal and alloparenting behavior. . . . . . . .
Warning: parenting success is influenced by the environment. . . . . . . . . . . . .
Role of environmental and maternal variables on paternal care . . . . . . . . . . . .
Hormonal/neuropeptide mediators of paternal behavior. . . . . . . . . . . . . . . . . .
Role of stress on monogamy and paternal care . . . . . . . . . . . . . . . . . . . . . . . . .
Neuropeptides/neurotransmitters and the rewarding aspects of parenthood?.
Further considerations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Limitations of smaller animal models. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Animal models of varying paternal structures . . . . . . . . . . . . . . . . . . . . . . . . . .
Common neural correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

* Corresponding author. Tel.: +1 403 220 4497; fax: +1 403 283 2700.
E-mail address: [email protected] (A.C. Kentner).
0149-7634/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2009.08.010

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A.C. Kentner et al. / Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

1. Introduction
In mammals, as in many species, reproductive success requires
that parents spend a substantial amount of energy feeding and
caring for their offspring. In the case of some mammals, parents
will provide for their offspring for periods that can last for years.
The study of parental behavior typically emphasizes the role of the
mother while minimizing the influence of the father. This is not
surprising given that the female’s role in lactation is presumed to
have resulted in her becoming the dominant care provider.
Nevertheless, the potential role of mammalian males in parental
care may be one of the most understudied topics in the literature,
and may be one that could provide important information about
optimal parental care in mammal species including our own, in
which the presence of caring fathers may determine a child’s
appropriate emotional and cognitive development (Phares and
Compas, 1992).
Interestingly, paternal care is present in many avian and fish
species, and in many of these species most parental investment is
provided by males (for reviews see Ziegler, 2000; Rosenblatt, 2003;
Whiteman and Coˆte, 2004). In the mammalian literature, examples
of paternal care have been described in various rodent and nonhuman primates, for example, prairie voles and the common
marmoset (Wang et al., 1998; Ziegler, 2000). In spite of this, and
because the occurrence of mammalian paternal care is relatively
rare, it is often difficult to assess paternal behavior. Previously, this
behavior had been scored as ‘maternal behavior’ but supplemented
by a male (see Brown, 1993; Mayer et al., 1979; Rosenblatt and
Ceus, 1998), and this reflects the necessity to properly differentiate
‘paternal behavior’ from ‘maternal behavior’ and to identify the
underlying mechanisms that mediate each, both separately and
together. Indeed, maternal and paternal behaviors, when available,
act together as a complimentary system, to ensure the health and
survival of offspring; however at this point, little is known of the
mechanisms underlying paternal care since most investigations
focus only on the maternal contribution. The following, therefore,
provides an overview of animal models of paternal behavior that
reflect parent–offspring interactions that occur in the human
population including alloparenting (adoptions) and even filicide.
Specifically, we will examine human parental systems and
paternal influences on offspring success. This will be followed
by an exploration of various animal models and the neuroendocrine and environmental influences that mediate paternal
behavior.
2. Parental investment and parental behavior
The concept of parental investment was coined to explain the
relationship between the costs of producing offspring and the
reproductive payoffs that are attained through these so called
investments (Trivers, 1972). The costs usually come in the form of
compromising future reproductive opportunities to maximize the
possibility that current offspring reach reproductive age. In
polygamous species, the direct costs of reproduction are incurred
by females, who must nourish offspring from conception to the
postpartum period and whose reproductive potential is restricted
by a limited number of ova. In males, reproductive investment is
associated with competition, territorial defense, and mate seeking.
While the reproductive potential of males is exponentially larger
than that of females, only a few males actually achieve
reproductive success. In monogamous mammals, mothers continue to invest energy in maternal care and nourishment while
delaying future reproductive efforts, yet fathers will also provide
for direct care of the young. Thus, parental investment is positively
correlated with parental care in these mammalian species.
Interestingly, game theory models suggest that in biparental

439

species, the reproductive benefits of paternal care outweigh the
reproductive costs of males not engaging in extra pair copulations
(McNamara et al., 2003). In other words, having a father around
will increase the chances of offspring survival in these species.
Similar models have identified a series of variables that may have
led to males of other species to show less parental behavior and
shifted to polygamy (Barta et al., 2002).
3. Human parental systems
Parental care, specifically paternal, appears to be related to the
mating system ingrained within the family structure, be it
culturally or genetically derived. In general, there are two main
types of human mating systems – monogamy (at least serial) and
polygamy (or promiscuity) – with the former system associated
with greater amounts of paternal investment in the form of direct
care, as determined by cross-cultural analysis (Marlowe, 2000); for
example, paternal care is greater if cohabitating with both
offspring and mother (Draper, 1989; Brunelli et al., 1995). The
dynamic of the typical family, however, has varied across
generations with the definition being challenged by factors
including death, divorce, gay marriage, adoption, and the
introduction of women into the workforce (Marsiglio et al.,
2000), all of which are mediated by cultural and economic
influences. This has lead to diverse parental structures which are
primarily made-up of either uniparental, biparental, or even
surrogate guardians who may or may not be genetically related to
the child. As a result, differential distributions of parental
responsibilities between families have arisen.
Historically, fathers in western societies dominated the workforce and were expected to have little direct-involvement in child
raising responsibilities, despite the imposed monogamous marriage system. This perspective continues with investigators
reporting inverse relationships between a father’s investment at
work and his child-raising responsibilities (McBride and Rane,
1997) which is likely true for mothers as well. The recent
phenomenon of maternal employment has posed a challenge to
this arrangement as it becomes apparent that the proportion of
father’s involvement with children (including engagement, accessibility, and responsibility) is increased when the mother is also
working (McBride and Mills, 1993). However, it is likely that this
increased proportion of responsibility may be due to mothers
participating less, as opposed to the father contributing more, in
child rearing responsibilities (McBride and Mills, 1993).
Importantly, the literature shows that despite the viewpoint
that mothers are better parents as a group, fathers can be just as
competent in caring for their children. Fathers, like mothers, learn
by doing, and the higher level of skill they perceive themselves to
have, the more involved they become with their young (see
McHale and Huston, 1984; Silverstein, 1996). Moreover, men more
often report that they would like to spend additional time with
their children (Milkie et al., 2004), and it appears that we are
currently in a transitional shift toward men becoming recognizable
caregivers in the home.
4. Human paternal influence and offspring success
Paternal influence results in various magnitudes of offspring
success and development. For example, the impact of paternal care
on health appears to be quite significant in both male and female
offspring as reported in a longitudinal study of a Caribbean village,
Bwa Mawego. Children separated from their biological father, or
living with a step-father, had higher cortisol levels, immunosuppression, and increased rates of illness than their half-siblings
living with both genetic parents (Flinn and England, 1997).
Therefore, the absence of paternal care may lead to either a

440

A.C. Kentner et al. / Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

hyperactive stress axis or to increased sensitivity to stressors,
making these children more susceptible to disease (Phares and
Compas, 1992).
Paternal behavior also has the potential to negatively affect
the success of offspring due to broken attachments, hostility,
and violence. In the case of absentee fathers, this form of
paternal conduct has been related to violent activity and crime
in some preadolescent males (see Ember and Ember, 1994),
although socialization for aggression is typically the most
significant predictor for interpersonal violence, through hostile
parenting (Cote et al., 2007). Indeed, in fathers who are in close
proximity to their offspring, ‘harsh’ parenting is a strong
predictor for male childhood aggression (Weiss et al., 1992;
Chang et al., 2003).
Despite the impact that a negative paternal influence can have
on offspring, paternal involvement is beginning to be recognized as
equally important as maternal influences in successful childhood
development, demonstrated by its positive correlations with
cognitive competence in school (see Forehand and Nousiainen,
1993; Dubois et al., 1994), as well as adult psychological
adjustment (Amato, 1994; Williams and Radin, 1999) in both
males and females. Specifically, in a systematic review by Sarkadi
et al. (2007), paternal engagement, that is, direct interaction with
the child including play and other care giving roles, was identified
to be more indicative of later positive childhood outcomes than
just accessibility to the father and paternal responsibility alone.
5. Paternal measurement issues
As can be deduced from above, human paternal influence, or
lack thereof, can significantly impact offspring, with the
potential for both positive and negative outcomes. In addition,
there appears to be several social variables that mediate the
amount of paternal investment available. One shortcoming in
this literature is a consistent measurement scale to describe
paternal behavior between studies. Thus, the question remains,
what constitutes human paternal behavior? In most crosscultural studies, actual measures of proximity to the child have
been used to assess human paternal investment, likely with the
unwarranted assumption that this is related to the quality of the
relationship (see Veneziano, 2003). It appears that when
assessed alongside physical availability, paternal warmth is a
stronger indicator of child behavior (Amato, 1994; Veneziano
and Rohner, 1998). When compared to maternal warmth on
scales of aggression, academic performance, and social competency, paternal warmth is a better outcome predictor (Chen et al.,
2000). Some typical behaviors that have been incorporated into a
measure of paternal warmth include verbal and physical
demonstrations—for example, singing, talking, comforting, as
well as hugging, and playing (Veneziano, 2003). However, it is
important to note that human paternal investment encompasses
several other types of behaviors such as planning, provisioning
through financial means, and protection, whether the father is
present with the child or not. In addition, it is likely that the
perception of paternal warmth, from the child’s perspective, is
more influential in offspring success.
A question that begins to emerge is whether the measurement
scales now utilized are viewed purely as paternal versus maternal
indicators, or if a more gender-neutral view of all parental
behaviors is being developed instead. One criticism regarding the
assessment of paternal involvement is that often a ‘mother
template’ is applied in order to appraise this behavior (see Stolz
et al., 2005). Stolz et al. (2005) subscribe to the view that maternal
and paternal dimensions are different, but complimentary, and
must be assessed individually. This is important in that paternal
behavior is not the mirror-image of maternal behavior.

6. Human paternal behavior and endocrine changes
Most of the influences on human paternal involvement
discussed thus far have been from the social realm; but recently
hormonal correlates have been investigated. Current research now
indicates that the hormone patterns observed in expectant fathers
residing with their partner may prime the onset of paternal
behavior, since such profiles are non-existent in nonpaternal
species (Storey et al., 2000). In a monogamous family structure,
men and women have been reported to demonstrate comparable
gestational hormone variations. For example, Storey and coworkers observed both parents to demonstrate elevated prolactin
and cortisol levels immediately prior to birth, followed by
diminished postnatal estradiol and testosterone levels in mothers
and fathers respectively (2000). Berg and Wynne-Edwards (2001)
reported higher estradiol levels in expectant and new fathers
whereas this hormone was undetectable in most of the men in the
control group. In addition, estradiol concentrations showed
individual increases during the last phase of pregnancy, and into
the first month after childbirth, although its role in paternal
behavior has not been determined (Berg and Wynne-Edwards,
2001). Other work by this group, using time- and day-matched
samples, has shown that salivary hormone concentrations of
estradiol and testosterone in nine sets of soon-to-be and
subsequently new parents were not correlated, although cortisol
responses were. In mothers, cortisol increased as the parturition
date approached, an increase observed in fathers one week prior to
the birth. However, these changes could be attributable to shared
environmental circumstances (Berg and Wynne-Edwards, 2002).
Unfortunately, absent in this study was a group of couples who
were not expecting a child. However, in line with other work, Berg
and Wynne-Edwards (2001) did report reductions in paternal
salivary testosterone levels during the last few months of their
partner’s pregnancy, which continued throughout the initial
postnatal period. This suppression of testosterone level has been
hypothesized to reduce aggression toward the infant offspring
(Perrigo et al., 1991), although such findings have not been tested
directly in humans. Interestingly, paternal experience is related to
hormone changes in response to infant stimuli. For example,
testosterone levels have been shown to increase when both
experienced and first-time fathers are introduced to the crying
stimuli of genetically unrelated infants (Fleming et al., 2002;
Storey et al., 2000). In this work, fathers with more experience with
infants had lower testosterone and higher progesterone levels in
response to a crying baby stimulus. Fathers with lower testosterone levels reported an increased need to respond to the crying
infant stimulus (Fleming et al., 2002) while fathers with higher
prolactin levels responded to ‘hunger’ cries more positively (Storey
et al., 2000). With respect to paternal experience, experienced
fathers showed larger increases in prolactin following presentation
to infant stimuli (Fleming et al., 2002; Delahunty et al., 2007) and
first-time fathers were reported to have decreased prolactin levels
after exposure to infant cues (Storey et al., 2000). Moreover, men
with more than one younger sibling demonstrated this increased
prolactin response while men with fewer siblings had a decrease in
prolactin following infant contact; this is suggestive that prolactin
levels were dependent on prior experience with infants (Delahunty
et al., 2007).
The oxytocin system is involved in attachment and is
considered integral to reproduction and parental behavior (see
Insel, 1992). Henry and Wang (1998) propose that stress interferes
with the underlying mechanisms of attachment by chronically
activating catecholamines; this may be a way by which social
stressors affect the endocrine system, thus influencing paternal
behaviors, and even aggression. Indeed, in one study examining the
nature of paternal filicide in Fiji, convicted fathers tended to be

A.C. Kentner et al. / Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

from poor socioeconomic backgrounds and were concurrently
experiencing marital disruptions (Adinkrah, 2003). Additionally,
elevated parental stress places fathers, and not just mothers, at risk
for postpartum depression (Goodman, 2004), perhaps in part
through downregulated oxytocin activity that may accompany
situational stressors. Indeed, poor social functioning and lower
economic status have been identified as risk factors for paternal
depression (Areias et al., 1996) and maternal postpartum
depression is known to subsequently result in disrupted attachments with infants (Milgrom and McCloud, 1996); the same is
likely true of postpartum fathers and their children, resulting in
compromised offspring success. For example, children of fathers
who suffered from depression during both the pre and postpartum
periods showed disrupted behavioral and emotional development
at 3.5 years of age while children whose fathers suffered from
depression postnatally scored higher on a conduct problems scale
(Ramchandani et al., 2008).
An important consideration is the problem of interpreting the
role of oxytocin, and other hormones, in humans with respect to
attachment and other behaviors. Human parental behavior is
influenced by cultural and environmental factors making it
difficult to determine the relative contribution of hormone profiles
to human parental behaviors (McCarthy and Altemus, 1997; Young
and Insel, 2002); therefore investigators often turn to animal
studies in order to assess the role of the endocrine and nervous
systems on human paternal investment and mating systems.
7. The model animal
As with most animal models of behavior, there is great diversity
in the types of parental care offered across species, and these
differences appear to be rooted to ecological requirements and the
species mating system. In several mammalian species, the
monogamous system of pair bonding consists of an adult male
and female that mate and share parental care, including nest
guarding. Such relationships are complicated further by DNA
fingerprinting studies demonstrating that acting fathers are not
always the genetic father despite a biparental affiliation (Garza
et al., 1997; Petrie and Kempenaers, 1998). In the polygynous
system, animals typically join with a mate only for the actual act of
copulation (described in Young et al., 1998).
Although rare in mammals, paternal behavior is more common
in parental fish species (Perrone and Zaret, 1979), and has been
reported to occur in invertebrates (Thornhill, 1976). Paternal
investment occurs in over 90% of birds and is thought to be the
ancestral form of parental behavior before maternal care evolved
(Van Rhijn, 1990). Recent evidence has also emerged showing that
some dinosaur species, related to birds, may also have been
primarily paternal (see Prum, 2008). Although these paternal
models are important, the current focus will be on mammals.
In mammals, paternal behavior has been measured in tamarins
(Ziegler et al., 2004), marmosets (Almond et al., 2006), gerbils
(Piovanotti and Viera, 2004), hamsters (Hume and WynneEdwards, 2005), and most commonly in voles (Young et al.,
1998; Storey and Snow, 1987; Oliveras and Novak, 1986) and mice
(Trainor and Marler, 2001). Please refer to Table 1 for a list of
common paternal versus nonpaternal species.
The California mouse is a biparental species with the pairbond
remaining together for multiple breeding seasons (Ribble, 1991).
Paternal behavior in this species is quite involved in that fathers
spend amounts of time comparable to that of the mother caring for
the pups (see Gubernick et al., 1993). This paternal model has been
contrasted, in behavioral and neurobiological studies, to that of the
white-footed mouse which is a polygamous group that offers very
little paternal care (Bester-Meredith et al., 1999). Pup retrieval is
low between both of these mouse species; however California mice

441

spend more time retrieving pups around postnatal day 21 and will
huddle and lick their offspring over the first two weeks after birth.
Comparatively, the white-footed mouse spends more time outside
of the nest (Bester-Meredith et al., 1999).
Another model of paternal behavior is the prairie vole. Unlike its
promiscuous counterpart, the montane vole, the prairie vole male
will form a bond with its female mate that will last beyond
copulation; in addition, he will participate in parental duties until
the pups leave, long after weaning (see Young et al., 1998). In terms
of establishing this high partner affiliation, Insel et al. (1995)
determined that a 24-h period of mating was required for this
bond. Aggression was also increased in male prairie voles following
a 24-h period of mating, compared to males exposed to either
social (not sexual) contact, or social isolation. This group also
reported that neither 1 nor 6 h of mating exposure was sufficient to
increase aggressive responses to intruders. Notable was the
observation that paternal behavior was generally high in all males
regardless of mating experience suggesting that they are
constitutionally adapted for fatherhood (Insel et al., 1995). In
male prairie voles, mating is necessary to facilitate the formation of
pair bonding and to increase aggression, perhaps for partner and
nest/pup guarding; these behaviors do not accompany mating in
the promiscuous montane vole (Insel et al., 1995).
Other vole species, such as the pine and meadow voles, have
also been used to assess paternal behavior; however they tend to
be more similar to each other in this respect than that observed in
the prairie and montane voles. The pine and meadow voles are
monogamous and polygamous, respectively (see Salo et al., 1993)
and show paternal care indirectly through food cashing and nest
construction (Oliveras and Novak, 1986). Overall, the vole species
are recognized as demonstrating categorical levels of paternal
behavior, with the prairie vole showing the most direct paternal
care, followed by the pine vole, and finally the meadow and
montane voles participating in almost no paternal care (see
Oliveras and Novak, 1986).
The role of hormones in the induction of paternal behavior has
been demonstrated in a number of rodent species including some
in which males do not engage in paternal behavior. In these
studies, male animals are castrated, and may then receive gonodal
sex steroid treatment mimicking the hormonal milieu of a female
to induce changes in aggression, social bonding, and paternal
behavior. It has been shown that neonatal, as opposed to adult,
castration can reduce infanticide in rats (Rosenberg et al., 1971).
Moreover, estrogen administration has been reported to stimulate
parental behaviors such as crouching, anogenital licking, sniffing,
and pup retrieval in nonpaternal rats (Rosenblatt and Ceus, 1998).
The span of behaviors offered by these models provides
valuable information for the functioning of neurobiological and
hormonal pathways that account for different behavioral manifestations of paternal care and mating behavior.
8. Nest cleaning: measurement of paternal and alloparenting
behavior
Accompanying the animal models above are some well
established measures of parental behavior. Interestingly, the
descriptions of these measures have oftentimes been illustrated
as ‘maternal behaviors’ that are enacted by a male, particularly
when assessed in animal models that are not typically paternal, or
have been hormonally feminized (see Brown, 1993; Mayer et al.,
1979; Rosenblatt and Ceus, 1998). This view is mistaken given that
even in the rat juvenile males will spontaneously help their mother
in rearing younger siblings without the administration of
hormones or other interventions (Mayer et al., 1979; Rees and
Fleming, 2001; Rees et al., 2005). The same occurs in adult male
rats, although initiation of these alloparenting or paternal

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Table 1
List of common paternal versus nonpaternal species.
Typical animal model

Monogamous/
promiscuous

Paternal/nonpaternal

Examples of groups employing this model

Cotton-top tamarin (Saguinus oedipus)
and Golden lion (Leontopithecus rosalia)

Monogamous

Paternal

Rapaport (2006), Sussman (2000), Ziegler et al. (2004)

Marmoset (common (Callithrix jacchus)
and black tufted-ear (Callithrix pennicillata))

Monogamous

Paternal

Almond et al. (2006), Nunes et al. (2001), Pryce et al. (1993)

Meerkat (Suricata suricatta)

Monogamous

Paternal

Brotherton et al. (2001), Carlson et al. (2006)

Djungarian hamster (Phodopus campbelli)

Monogamous

Paternal

Timonin and Wynne-Edwards (2008), Wynne-Edwards
and Lisk (1989)

Siberian hamster (Phodopus sungorus)

Promiscuous

Nonpaternal

Timonin and Wynne-Edwards (2006)

California mouse (Peromyscus californicus)

Monogamous

Paternal

Gubernick et al. (1993, 1994, 1995), Gubernick and
Nelson (1989), Gubernick and Teferi (2000);
Marler et al. (2005), Trainor and Marler (2001, 2002)

House/wild-type mouse (Mus musculus)

Promiscuous but
will cohabitate
with female in
laboratory

Paternal—but dependent
on strain and stock specific

Huck et al. (1982), Perrigo et al. (1989, 1990, 1991)

White-footed mouse (Peromyscus leucopus)

Promiscuous

Nonpaternal—will show
facultative care

Bester-Meredith et al. (1999), Bester-Meredith
and Marler (2003)

Prairie vole (Microtus ochrogaster)

Monogamous

Paternal

Bamshad et al. (1994), DeVries et al. (1996, 2002),
Insel et al. (1995), Insel and Hulihan (1995), Insel
and Shapiro (1992), Lim et al. (2006), McGuire (1988),
Wang (1995), Wang et al. (1994, 1997, 2000)

Guenther’s vole (Microtus guentheri)

Monogamous

Paternal

Libhaber and Eilam (2002)

Pine vole (Microtus pinetorum)

Monogamous

Paternal (less so than
Pine vole)

Lim et al. (2006), Oliveras and Novak (1986), Salo et al. (1993)

Meadow vole (Microtus pennsylanicus)

Promiscuous

Nonpaternal—will show
facultative care

Lim et al. (2006), McGuire (1988), Oliveras and Novak (1986),
Parker and Lee (2001, 2002), Salo et al. (1993), Storey
and Snow (1987)

Montane vole (Microtus montanus)

Promiscuous

Nonpaternal

Insel et al. (1995), Lim et al. (2006), Oliveras and Novak (1986),
Salo et al. (1993), Shapiro and Insel (1990),
Wang et al. (1997, 2000), Young et al. (1998)

Rat (Rattus norvegicus)

Promiscuous

Nonpaternal

Rosenberg et al. (1971), Rosenblatt (1967), Rosenblatt
and Ceus (1998), Mayer et al. (1979)

Goeldi’s Monkey’s (Callimico goeldi)

Monogamous

Paternal

Schradin and Anzenberger (2003)

Mongolian Gerbils (Meriones unguiculatus)

Monogamous

Paternal

Elwood and Ostermeyer (1986), Piovanotti and Viera (2004)

behaviors takes longer periods of sensitization (approximately 10
versus 3 or 4 days in juveniles) to appear (Mayer et al., 1979).
Recently, such behaviors have been described under the common
umbrella of ‘parental behavior’ (Lonstein and Fleming, 2007),
although much of the research still focuses primarily on maternal
behavior, or sometimes hormone-treated, feminized males, at least
in the rat (see below).
In mammals, two factors distinguish between males and
females in terms of parental ability: parturition and lactation.
However, there are some exceptions. For example, the male Dayak
fruit bat is reported to lactate, although there have been no
observations to date of the males of this species nursing young
(Francis et al., 1994). Of additional note, paternally active hamsters
are known to assist in all aspects of the delivery of their offspring
(Jones and Wynne-Edwards, 2000). Indeed, most studies do not
assess paternal behavior during parturition (Jones and WynneEdwards, 2000), but instead reunite fathers and offspring after
birth, or assess paternal care via foster pups. Still, in assessing both
maternal and paternal behavior (in rodent models), the same
established protocols are followed. Examples of measures include,
but are not limited to: the amount of time contributed to, and
quality of grooming (pup licking), thermoregulatory behaviors
such as huddling or crouching, duration to retrieve displaced
young to the nest, and quality of nest building (Trainor and Marler,

2001; Rees et al., 2005; see Lonstein and Fleming, 2007). In
addition, some investigators record passive association with
offspring, such as the amount of time spent sleeping in the nest,
as well as time spent away from the nest engaging in other
behaviors such as wheel running and resting (Trainor and Marler,
2001).
Indicators of paternal behavior, in addition to behaviors that are
initiated following the birth of, or exposure to offspring, also
include preparatory behaviors such as nest building and food
gathering. This type of behavior has been attributed to courtship
during which the male ensures that the female mate is not already
impregnated (Dawkins, 1989). However, in many species, it is the
female who selects her partner (see Geary, 2000), raising doubt to
this assertion.
Beyond species-typical parenting, there are several protocols
that have been developed to evaluate the motivational preferences
for pups in rats and mice. One test is the unconditioned place
preference test between pup-related and non-pup related stimuli.
In this procedure, the proportion of time spent in the different
areas where the stimuli are located is determined; an adaptation of
this procedure is the conditioned place preference test (see
Lonstein and Fleming, 2007).
Another frequently used assessment of parental motivation is
the operant lever press in which each lever press results in the

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presentation of a pup (Lee et al., 2000; Lonstein and Fleming, 2007),
although this paradigm does not appear to have been used with
male animals. In animal models using primates, behaviors such as
allogrooming and visual tracking can be used as indicators of
attachment (Kraemer, 1997). Many of the studies described later
utilize these outlined procedures, although the protocols for
assessing motivation are rarely used in investigating paternal
behavior.
Most experiments assess maternal and paternal behavior
separately, and as a result may overlook important behaviors.
For example, in one laboratory observation with the Guenther’s
vole, a biparental species, both maternal and paternal behaviors
were in part mediated by ‘forced babysitting’. In this occurrence,
when one vole left the nest and intercepted its partner outside of
the nest-area, the animal used its incisors to ‘drag’ its partner back
to the nest, presumably to care for the young. Half of the time, the
‘dragged’ partner did not remain in the nest, and this behavior
continued until one partner acquiesced (Libhaber and Eilam,
2002). Although typically instigated by the male, females too have
been shown to force their partners to babysit. The mechanisms
underlying this behavior are unknown (Libhaber and Eilam, 2002).
Babysitting behavior in cooperative breeding systems such as
the mongoose demonstrates that male care is not restricted to
fathers. In these systems, dominant breeding pairs rarely remain in
the natal nest while the rest of the pack forages; instead the
energetic cost is left to subordinate male and females. These
subordinates are usually adult siblings and offspring of the
breeding female; however non-relatives such as immigrants to
the group have also been observed to guard (Clutton-Brock et al.,
1998). With respect to meerkats, offspring survival is not
compromised by a smaller group size in which the group members
take on more work (Clutton-Brock et al., 1998), while the average
number of babysitters is directly related to pup survivorship in the
banded mongoose (Cant, 2003). In these cooperative systems there
is no sex difference in total babysitting contribution nor were
helpers forced to babysit (Cant, 2003; Clutton-Brock et al., 1998).
Instead, babysitting behavior in meerkats was often provided by
heavier individuals (Clutton-Brock et al., 1998) thus babysitting
behavior may be mediated by nutritional state (see Cant, 2003).
In a field study assessing the parental behaviors of a
promiscuous squirrel species, in which paternal care would not
normally be expected to occur, Huber et al. (2002) report that
observed digging behaviors in litter burrows was an indirect
paternal effort that resulted in significantly higher offspring
weight when pups emerged from the nest. This finding was related
to observations that mothers that had a male digging at her burrow
spent more time foraging than females without a male present at
her nest (Huber et al., 2002). Together, these studies underline the
importance of assessing maternal and paternal care as a
complimentary system, as well as separately.
9. Warning: parenting success is influenced by the
environment
The motivation and ability of mammalian paternal behavior to
contribute to offspring success appears to be not only a function of
interspecies genetic differences but can also be affected by the
environment. Moreover, it has been thought that paternal behavior
emerged in some species to ensure offspring survival. For example,
Storey and Snow (1987) conducted an experiment demonstrating
that paternal attendance in the meadow vole was reduced when
another male was housed near the nest; potentially due to paternal
uncertainty. In addition, offspring survival and weight were
compromised with reduced paternal presence at the nest. Field
studies with the California mouse demonstrate compromised
survival of pups when the father is absent (reviewed by Gubernick

443

and Teferi, 2000). Laboratory studies reveal similar findings with
the Djungarian hamster; survival rates of the litters are decreased
by almost half in the absence of the father and reduced even more
when room temperature is lowered to 4 8C (Wynne-Edwards and
Lisk, 1989). It appears that the main function of the father is to
provide warmth, although in nonpaternal Siberian hamster litters,
ambient temperature changes in the absence of the father do not
significantly affect litter size (Wynne-Edwards and Lisk, 1989).
Some species which are not typically paternal will become so
when environmental conditions become difficult; this is known as
‘facultative care’ (see Parker and Lee, 2002). In the case of the
meadow vole, this species has been reported to nest with its mate
and invest more in its offspring during the colder months,
presumably to maintain thermoregulation (Parker and Lee, 2002).
Indeed, previous studies have shown variations in maternal care as a
function of nest temperature in laboratory rats (Jans and Woodside,
1990; Woodside and Jans, 1988; Woodside and Leon, 1980). Results
from these studies clearly show that the heat produced by maternal
contact with the pups shortens the duration of mother/litter contact.
Furthermore, manipulations that artificially increase nest temperature or room temperature lead to shorter mother/litter contacts.
Whether male rats will show increased contact with pups in
response to drops in temperature is unknown.
The role of photoperiod also influences the behavior of the nonparental male in some species. As mentioned, the meadow vole
will begin biparental care during the colder months of the year
(Parker and Lee, 2001, 2002), when there is a significant shortening
of day length. Sexually naı¨ve male meadow voles housed in short
day length conditions are more responsive to pups in terms of
retrieval, grooming, and huddling, than their long day lightexposed counterparts (Parker and Lee, 2001). Under laboratory
conditions, rearing meadow vole pups with both parents does not
increase survival rate, only pup weight (Storey and Snow, 1987).
Interestingly, ‘crisis-initiated’ paternal behaviors may beg the
question of whether or not the quality of the maternal instinct is
compromised, or enhanced in the presence of the father.
Previous pup experience can also affect subsequent paternal
behavior as demonstrated by the ability of repeated pup exposure
to induce parental behavior in virgin male and female rats
(Rosenblatt, 1967; Rosenblatt and Ceus, 1998). Prior experience
also has a role in establishing paternal disposition toward
biological offspring. For example, meadow voles that were
cross-fostered to biparental prairie voles received more paternal
care than their meadow vole counterparts that were raised by
other meadow voles. When the cross-species fosters became
adults, these male fathers spent more time with their biological
pups than meadow voles that were raised by their own species
(McGuire, 1988). This proposed ‘paternal learning model’ also
works in the opposite direction; male California mice, typically a
biparental species, that were retrieved less often by white-footed
mice foster parents were less effective at retrieving their own
young when parents themselves (Bester-Meredith et al., 1999). In
addition, these cross-fostered California mice had aggressive
temperaments that mimicked their less aggressive foster parents
more than that of their biological species (Bester-Meredith et al.,
1999). In turn, the offspring of these animals may display modified
paternal involvement, suggesting the potential for intergenerational transmission of behavior (see Marler et al., 2005), an area
receiving a lot of attention in the corresponding human research,
particularly with respect to maternal influences on maternal
aggression (for example, Conger et al., 2003). In the animal studies
of Bester-Meredith et al. (1999), a subsequent investigation
indicated that aggressive tendencies in a resident–intruder
paradigm were positively correlated with the amount of time
that fathers spent retrieving their pups, as opposed to any maternal
factors (Bester-Meredith and Marler, 2003).

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10. Role of environmental and maternal variables on paternal
care
Temperature and photoperiod also influence females which
may affect paternal behavior. For example, female meadow voles
are territorial during the summer, but allow males to nest with
them and their offspring in the colder months (see Parker and Lee,
2002). In the field, the female meadow vole may drive away the
father in order to prevent infanticide, a behavior that subsides with
either the changing temperature or light cycle. However, other
studies have reported that paternal behavior in the CD-1 mouse
strain is dependent on the presence of an aggressive female mate
(Maestripieri and Alleva, 1991) although this relationship has not
been observed in Swiss-Webster mice (Palanza and Parmigiani,
1991). Interestingly, brief cohabitation with a female, without
mating, significantly decreased the latency of paternal behavior
initiation in short day housed meadow voles (Parker and Lee,
2001).
In Goeldi monkeys, mothers direct threat vocalizations toward
fathers when they initiate contact with infants. Fathers then stop
touching the infant and even withdraw from their offspring
(Schradin and Anzenberger, 2003). Consequently, during the first
three weeks of life the mother exclusively carries the infant despite
the father’s apparent interest. This interest is determined by the
father initiating more body contact with the mother and infant pair
than with the mother prior to birth. Furthermore, this body contact
with the mother decreases when the father begins to carry the
infant. In one study, when a potential predator (a ferret) was
introduced into the environment, the latency for paternal care was
shortened by approximately 10 days, presumably because mothers
reduced threat vocalizations toward the father that was observed
carrying the infant (Schradin and Anzenberger, 2003).
11. Hormonal/neuropeptide mediators of paternal behavior
The first experiments to implicate the role of hormones in
parental behavior were reported by Terkel and Rosenblatt (1968,
1972). They transfused blood from a pregnant rat into virgin
females and were able to elicit maternal behavior. Since this
observation, there has been an explosion of interest in the role of
the endocrine system in the initiation and maintenance of parental
care (Table 2). Historically, many studies investigated the role of
hormones in the female rat, and then later studies included the
male rat. According to Brown (1993), parental care in male rats was
originally referred to as ‘maternal behavior’ by McQueen-Williams
in 1935, and following this, male rats were often demasculinized
and treated with hormone therapy in order to induce ‘maternal
behavior’ (reviewed in Brown, 1993). More recent studies tend to
investigate ‘paternal’ behaviors in naturally occurring animal

models of parental care. Still, it is important to reiterate that
paternal and maternal care are typically evaluated in isolation
from one another, although the real profile of parental care is likely
better understood when they function together as a complimentary system.
It has generally been established that testosterone levels
increase prior to birth, but dramatically decrease at the time of
parturition in rodent species that show paternal behavior (Brown
et al., 1995; Reburn and Wynne-Edwards, 1999). In CF-1 mice,
administration of testosterone induces infanticide, whereas
castration reduces this occurrence. Therefore decline of peripheral
testosterone is thought to prevent infanticide (Perrigo et al., 1989),
although aggressive behavior is generally increased in paternal
models (Trainor and Marler, 2001), likely for nest guarding.
However, Trainor and Marler (2001) observed that administration
of testosterone is able to stimulate parental behavior in male
California mice, noting that this hormone is subsequently
aromatized into estradiol, which itself also induces maternal
behavior in male animals when implanted into the medial preoptic
area (see Rosenblatt and Ceus, 1998). Indeed, gonadectomized
male California mice treated with an aromatase inhibitor in
combination with testosterone had lower levels of huddling and
pup grooming (Trainor and Marler, 2002). Although, none of the
male prairie voles treated with either a subcutaneous injection of
testosterone propionate, flutamide (an anti-androgen receptor
blocker), or an aromatase inhibitor displayed compromised
paternal behavior (Lonstein and De Vries, 2000) indicating either
species, or underlying procedural differences.
Timonin and Wynne-Edwards (2008) demonstrated a developmental role of estradiol in a biparental dwarf hamster species.
Hamsters were treated with letrozole, an aromatase inhibitor for
three days beginning at postnatal day 18, 34, or 90. Males treated
on postnatal day 18 demonstrated less paternal care such as
huddling, whereas hamsters treated at 34 and 90 days of age
exhibited compromised reproductive behavior and slight increases
in midwifery participation respectively. This work points to the
importance of critical windows in evaluating hormone and drug
effects on behavior.
One study employing estrogen receptor-a knockout mice
concluded that infanticide and aggression are mediated via two
separate mechanisms (Ogawa et al., 1998). Essentially, estrogen
receptor-a deficient mice did not initiate attacks in a resident–
intruder paradigm, even following daily administration of
testosterone propionate; in the gonadectomized wild-type mouse,
this procedure was able to reinstate aggression. However, rates of
infanticide were significantly higher in the knockout mice,
compared to their wild-type counterparts. This lead the investigators to propose that testosterone administration was able to
maintain infanticide behavior through androgen receptors, or

Table 2
Summary of hormone/neuropeptides and general effects on paternal behavior.
Hormone/neuropeptide

General role in paternal behavior
High levels (endogenous or administered)

Low levels (endogenous or inhibited)

Testosterone

" Infanticide in CF-1 mice (Perrigo et al., 1989).
" Paternal behavior in California mice (Trainor and Marler, 2001)
No effect in prairie voles (Lonstein and De Vries, 2000).

# Infanticide in CF-1 mice (Perrigo et al., 1989).

Estradiol
Progesterone
Prolactin

" Rat paternal behavior (Rosenblatt and Ceus, 1998).
" Pup aggression in house mice (Schneider et al., 2003).
" Paternal care in biparental hamster (Reburn and
Wynne-Edwards, 1999).
No effect in common marmoset (Almond et al., 2006).
Associated with maternal care
" Paternal care in prairie voles (Wang et al., 1994).
" Paternal care in meerkats (Carlson et al., 2006).

Oxytocin
Vassopressin
Corticosterone
Urocortin

" Paternal care in house mice (Schneider et al., 2003).
# Paternal care in biparental hamster
(Reburn and Wynne-Edwards, 1999).

# Paternal care in prairie voles (Wang et al., 1994).
" Paternal care in tufted-ear marmoset (Nunes et al., 2001).
" Paternal care in prairie voles (Samuel et al., 2008).

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estrogen receptor-b, whereas intruder aggression itself is likely
mediated through estrogen receptor-a (Ogawa et al., 1998).
However, the authors did point out that infanticide is not always
correlated with peripheral testosterone levels (see Gandelman and
Vom Saal, 1975).
Although estradiol administration is recognized to initiate
parental behavior (see Rosenblatt and Ceus, 1998), endogenous
concentrations of this hormone were not altered in the biparental
Dwarf hamster species but were reported to increase prior to birth
and during offspring development in the non-parental Siberian
hamster male, with a noted decrease around birth (Schum and
Wynne-Edwards, 2005). While a decrease in progesterone had
been hypothesized in the biparental hamster, the inverse occurred
during late gestation and early pup development (Schum and
Wynne-Edwards, 2005). This was an unexpected result since
progesterone appears to have an inhibitory effect on paternal
behavior. Indeed, progesterone antagonism increased paternal care
in male house mice while administration of this hormone increased
aggression toward pups. Moreover, progesterone receptor knockout
mice were less aggressive toward young and did not demonstrate
infanticidal tendencies (Schneider et al., 2003).
Plasma prolactin levels have also been implicated in paternal
care. For example, in a biparental Dwarf hamster species, prolactin
levels increased one day after parturition, and males of this species
that failed to retrieve their young were associated with lower
levels of this hormone (Reburn and Wynne-Edwards, 1999).
Gubernick and Nelson (1989) also reported elevated prolactin
levels in male California mouse fathers, two days post partum.
Causing confusion with respect to the robustness of prolactin in
paternal care, oral administration of cabergoline, a dopamine
agonist that acts on D2 receptors consequently inhibiting prolactin
production, had no effect on paternal behavior in common
marmosets. However, there was a corresponding increase in
grooming behavior aimed at, and received by the female mate
(Almond et al., 2006). Moreover, similar observations were
reported for Djungarian hamsters, with regards to paternal care
(Brooks et al., 2005). Prolactin may increase in some hamster
species, but perhaps it may be involved in other behaviors such as
postpartum mating (see Reburn and Wynne-Edwards, 1999) and
not parental care. Overall, it is difficult to find consistent prolactin
hormone profiles tied to specific parental behaviors across species.
Both oxytocin and vasopressin have been widely recognized as
neuropeptides for affiliation. The architecture of these two
peptides is very similar, and both are released from magnocellular
neurons in the supraoptic nucleus, the paraventricular nucleus,
and the bed nucleus of the stria terminalis. From these sources,
oxytocin and vasopressin enter into the pituitary for later secretion
into the blood stream (see Carter, 1998 for review). There are four
recognized receptors responsible for the behavioral actions of
these peptides; one is associated with oxytocin, and the remainder
with vasopressin (V1a, V1b, V2), although both peptides may
cross-react with the other’s receptors (see Carter, 1998). Humans
and other primates have a circadian rhythm associated with
oxytocin circulating in the CSF, but not in plasma; no circadian
rhythms exist for oxytocin in rodents (see Amico et al., 1983; see
also, McCarthy and Altemus, 1997).
Oxytocin is paramount to the process of muscular contraction
during birth, and for milk let-down in postpartum mothers. Over the
past decade, interest in oxytocin has begun to shift from a primarily
female focus, to that of male affiliative behavior. Male mice lacking
oxytocin receptors make fewer ultrasonic vocalizations during
social isolation than wild-type controls; as adults, oxytocin-receptor
knockout males showed elevated aggression levels, similar to males
deficient in the oxytocin ligand (see Takayanagi et al., 2005). In a
cross-species comparison of prairie and montane voles, prairie vole
pups made ultrasonic vocalizations more frequently in response to

445

social isolation than montane voles under the same conditions
during the first two weeks of life (Shapiro and Insel, 1990). In
addition, plasma corticosterone levels were elevated half an hour
following separation in prairie voles, but remained stable in infant
montane voles. Qualitative amounts of parental care did not account
for these differences because montane vole infants cross-fostered to
prairie vole parents did not alter their behavioral responses (Shapiro
and Insel, 1990). In short, the montane vole infants seem comparable
to the oxytocin receptor knockout mice (Takayanagi et al., 2005) and
differences in oxytocin may underlie differences in affiliative
behavior in these species.
Using autoradiography techniques, Parker et al. (2001) mapped
the distribution of vasopressin and oxytocin binding in the brain of
experienced versus inexperienced meadow voles that participated
in facultative paternal behavior. Essentially, facultative paternal
males had higher levels of vasopressin binding in the olfactory
nucleus, and lateral septum, and higher levels of oxytocin in the
bed nucleus of the stria terminalis, and lateral amygdala than that
measured in the paternally inexperienced males, similar to what
has been observed in paternal vole species (Parker et al., 2001).
Plasma levels of oxytocin have been measured across the
reproductive cycle of expectant California biparental mouse
fathers, versus current fathers, or virgin males of the same species
(Gubernick et al., 1995). Oxytocin levels were reported to be higher
in expectant fathers the day following mating, with levels
declining by the twentieth day of gestation and thereafter
remaining comparable to the other male groups. One interpretation is that this peptide may not be directly involved in the
initiation of paternal care (Gubernick et al., 1995); in line with this,
Wang et al. (2000) failed to observe any increases in oxytocin
hypothalamic gene expression in either male prairie or montane
voles following the birth of their offspring, although increases were
measured in the female partner of both species. Hypothalamic
vasopressin gene expression was elevated in both males and
females of the biparental prairie vole species, but not in the
montane vole; it was suggested that oxytocin may be dominantly
related to female care while vasopressin is more affiliated with
paternal behavior (Wang et al., 2000). This reasoning is consistent
with the observation that oxytocin antagonists, but not vasopressin antagonists, are able to disrupt pair bonding and maternal care
in female prairie voles (Insel and Hulihan, 1995; Olazabal and
Young, 2006). Vasopressin infused into the lateral septum induced
dose dependent effects on paternal behavior with sexually naı¨ve
prairie voles exhibiting increased contact and crouching over pups
during a 10-min test period; these parental behaviors were
preventable by pre-administration of a V1a receptor antagonist
(Wang et al., 1994).
Despite the assumption in the literature that vasopressin is
directly related to paternal behavior, the data more adequately
support relative species differences in immunostaining and
receptor distribution of this peptide (Bester-Meredith et al.,
1999). For example, it was suggested that the male biparental
California mouse would have lower levels of vasopressinimmunoreactive staining in the bed nucleus of the stria terminalis,
as well as lower receptor density in the lateral septum (BesterMeredith et al., 1999), based on previous work comparing
monogamous and polygamous voles (Wang, 1995; Wang et al.,
1997). However, Bester-Meredith et al. (1999) observed higher
immunoreactive staining of vasopressin in both of these brain
regions in the biparental California mouse compared to that of the
white-footed mouse.
Irrespective of these differences in distantly related species, the
density of vasopressin-immunoreactive fibers was observed to
vary across the breeding cycle of the male prairie vole (Bamshad
et al., 1994). Shortly after mating, male prairie voles had the lowest
vasopressin fiber density in the lateral septum which corre-

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sponded to increases in paternal responsiveness. During early
gestation, and immediately after the birth of pups, fiber density
was at a moderate level reaching its highest values in sexually
naı¨ve males and late gestation (Bamshad et al., 1994). Reductions
in vasopressin immunoreactive fibers could be instigated by
cohabitation with an unfamiliar female, but not a male vole
(Bamshad et al., 1994).
Ultimately, the density of vasopressin fiber distribution is
dependent not only on the species but also on the specific brain
region involved. The distribution of vasopressin receptors and their
binding affinity were assessed using 125I-linear-vassopressin, a
ligand for the V1a receptor (Wang et al., 1997). After parturition
and continuing into adulthood, prairie voles exhibited higher
vasopressin receptor binding in the bed nucleus of the stria
terminalis and the amygdala than was apparent in montane voles
(Wang et al., 1997). However, in the lateral septum, both vole
species had low binding levels at birth, but the montane vole
exhibited increased binding during development, whereas the
prairie vole did not. This suggests that, at least in voles, receptor
binding is genetically or prenatally determined and may account
for organizational and behavioral differences between the species
(Wang et al., 1997). So it seems, at least in the biparental male
prairie vole, the low level of immunocytochemical staining in the
lateral septum is decreased even further upon mating, relating
vasopressin to partner preference and parental behavior (Bamshad
et al., 1994).
In the California mouse, the distribution of vasopressin
receptors is also plastic. When the pup retrieval rate by fathers
is experimentally manipulated, pups that are retrieved more often
have a higher density of immunostaining in the dorsal fiber tracts
of the bed nucleus of the stria terminalis, and less in the ventral cell
body-containing region (Frazier et al., 2006). This prior experience
is correlated to a decrease of aggression in the resident–intruder
paradigm, demonstrating that paternal behavior affects the neural
organization and behavior of offspring.
12. Role of stress on monogamy and paternal care
Gluccocorticoids are also implicated in monogamous species
that offer paternal care; parenthetically, the focus on sex hormones
has overshadowed the role of stress hormones in these attachment
systems. Still, their influence in paternal care is noted. For example,
lower titers of urinary estradiol, testosterone, and cortisol are
negatively associated with rates of infant carrying in the male
black tufted-ear marmoset suggesting that infant carrying is
mediated by stress via gluccocorticoid levels (Nunes et al., 2001).
Rises in plasma cortisol, but not prolactin or testosterone, are
positively associated with pup provisioning in subordinate male
meerkats (Carlson et al., 2006). Additionally, cortisol levels become
significantly reduced following the formation of a pair bond in
male Dwarf hamsters, but not in the uniparental Siberian hamster;
yet in the biparental model, cortisol concentrations increase
immediately prior to birth (Reburn and Wynne-Edwards, 1999).
Lim et al. (2006) cite a highly variable distribution of
corticotropin-releasing factor receptors (CRF1 and CRF2) between
monogamous and promiscuous voles. Employing in situ hybridization and immunocytochemisty techniques, this group examined
the allocation of two endogenous ligands for these receptors in the
brains of four vole species (prairie, pine, meadow, and montane).
Overall, they reported a highly conserved distribution of corticotropin-releasing factor and urocortin-1 within brain regions such
as the olfactory bulb, nucleus accumbens, medial preoptic area,
and bed nucleus of the stria terminalis, between each vole species,
suggesting an important role for receptor availability in pair
bonding and parental care (Lim et al., 2006). Treatment with either
corticotropin releasing factor (DeVries et al., 2002), corticosterone,

or exposure to forced swim (DeVries et al., 1996) is sufficient to
initiate partner preference in male prairie voles following 3 h of
cohabitation with a female. In the female prairie vole, these
preconditions inhibit the development of partner preference
(DeVries et al., 1996).
In the case of parental behavior, gluccocorticoids also appear to
be sexually dimorphic. For example, Bales et al. (2006) introduced
male and female prairie voles to either a swim test stressor or no
stressor. Forty-five minutes later, a parental care test was used to
assess behaviors such as huddling, licking and grooming, as well as
retrieval of pups after which plasma corticosterone levels were
determined. In males, the stress exposure facilitated paternal
behavior and corticosterone level was directly related to the
number of pup retrievals, but was negatively associated with
licking and grooming behaviors; female prairie voles did not alter
their parental care (Bales et al., 2006). This finding is consistent
with earlier data (Parker and Lee, 2001, 2002) of increased paternal
behavior under crisis situations, particularly evident in dominantly
non-parental male species.
Interestingly, Samuel et al. (2008) observed that intracerebroventricular administration of urocortin II was related to an increase
in the amount of passive parental behaviors such as huddling and
pseudohuddling in both male and female prairie voles, without
eliciting concomitant anxiety or locomotor effects. This increase in
passive parental care was likely not due to hypothermic effects of
treatment because administration of urocortin II, in rats, induced a
biphasic colonic temperature increase, peaking approximately
30 min and 4 h following exposure (see Telegdy and Adamik,
2008).
Most other studies relating stress peptides and paternal
behavior focus specifically on endogenous levels of corticosterone
under parental conditions. While one early study of naturally
paternal tamarins suggests that this hormone does not alter
parental behavior (Koranyi and Endroczi, 1987), work in male rats
indicates that corticosterone increases alongside the initial
avoidance to foster pups, but decreases with subsequent sensitization (Ziegler et al., 2004). Overall, these data suggest that
gluccocorticoids have differing effects between sex and species.
Further investigation is necessary to unveil the effects of stressors,
particularly severe ones, on paternal behavior.
As an aside, there are other types of neuropeptides and
transmitters involved in maternal care that may correspond to
paternal behavior as well, opening a door for future investigations.
For example, subcutaneous administration of prostaglandin F2
alpha has been implicated in the cessation of infanticide by
pregnant mice (McCarthy et al., 1986). In female mice that were
null for the dopamine b-hydroxylase gene, which consequently
eliminates norepinephrine and epinephrine, pup retrieval behavior
failed; however reinstating norephinephrine during late gestation
resulted in typical maternal behavior in subsequent litters by these
mothers (Thomas and Palmiter, 1997). Neither the roles of
norepinephrine, epinephrine, nor prostaglandin F2 alpha have
been reported in paternal behavior; their function in paternal care,
if any, remains unknown.
13. Neuropeptides/neurotransmitters and the rewarding
aspects of parenthood?
In 2003, Thomas Insel wrote an important paper highlighting the
question: is social attachment addictive? In it, he explored the role of
the mesocorticolimbic system and reward in attachment, concluding that this circuit is significant, at least in the context of maternal
behavior and pair bonding relationships in voles (Insel, 2003). Even
before this, Panksepp’s laboratory had been exploring the idea of
social reward and maternal–infant attachments as relating to
motivational systems (reviewed in Panksepp et al., 1997), although

A.C. Kentner et al. / Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

the work reviewed did not clearly distinguish between attachment
and the need for thermoregulation/nourishment in reward per se.
One such investigation involved the role of oxytocin and odor cues,
paired with maternal reunion, following a period of separation.
Fifteen-day-old pups that received intracerebral administration of
oxytocin approached an odor more quickly and spent more time
near the source of the odor when that scent had previously been
paired with maternal reunion; these behaviors were not observed in
pups that were administered the oxytocin antagonist (Nelson and
Panksepp, 1996). As an aside, if oxytocin were mediating infant–
maternal interactions via ingestive regulation systems, it would be
expected that oxytocin would decrease approach behavior toward
the odor since this peptide reduces fluid and food intake in adult rats
(Arletti et al., 1990).
Insel (2003) linked maternal behavior to reward with a focus on
the dopaminergic system. Insel suggested that one of the first
indications that motherhood might be rewarding is the observation that pregnant dams change from a fearfulness of pups to a
‘selective motivation’ toward them (see Insel, 2003). A more
quantitative way to assess this motivation is through operant
paradigms where female mice (Hauser and Gandelman, 1985), rats
(Lee et al., 2000; Lonstein and Fleming, 2007), and primates (Pryce
et al., 1993) will respond for infant stimuli. For example, Sprague–
Dawley rat dams that had a medial preoptic area, amygdala, or
nucleus accumbens lesion demonstrated disrupted retrieval
behaviors of pups following a lever press. The postpartum rats
with the medial preoptic area and amygdala lesion had severe and
slight deficits, respectively, in the instrumental task, whereas
nucleus accumbens lesion rats did not (Lee et al., 2000). These data
suggest that the preoptic area is critical for the elicitation of both
appetitive and consummatory maternal responses, whereas the
role of the nucleus accumbens may be important only for
consummatory maternal responses. As yet, it does not appear
that any study has directly investigated the motivational system of
a naturally paternal species, or whether operant behaviors can be
elicited from male animals for access to infant stimuli.
In maternal dams, interaction with rat pups increases dopamine
release within the ventral striatum (Hansen et al., 1993) and
treatment with 6-hydroxydopamine disrupts maternal behavior
by depleting dopamine levels in the nucleus accumbens and
ventral tegmental area (Hansen et al., 1991). Additionally, there is
c-Fos activation in the nucleus accumbens (Lonstein et al., 1998)
and lateral amygdala (Fleming and Korsmit, 1996), as well as Fos
activation along cells of the medial preoptic area projecting to the
ventral tegmental area and subsequently, the nucleus accumbens
(Numan and Numan, 1997) in maternal rats; all are sites
implicated in a proposed reward circuit underlying maternal
behavior (see Insel, 2003). Furthermore, lesions of these areas all
show deficits in maternal responding of postpartum rats (Numan
and Smith, 1984; Lee et al., 2000). It has also been shown that
intraperitoneal administration of a dopamine receptor antagonist,
haloperidol (at low but not high doses), in both parental male and
female prairie voles, reduced licking of pups and increased the time
for fathers to initiate contact with offspring, without compromising the activity level of the parents (Lonstein, 2002).
Many investigations into the rewarding aspects of affiliative
behavior in females focus on pair bonding relationships with
respect to the oxytocin and dopamine systems (see Insel, 2003).
This idea partly evolved from some of Insel’s previous work
showing the location of oxytocin receptors in brain regions
associated with reward, such as the nucleus accumbens and
prelimbic cortex (Insel and Shapiro, 1992; Insel, 2003). Questions
of interest stemming from this work include: (a) are the reward
circuits involved in maternal care and pair bond affiliation
identical to each other, and further, (b) are they similarly involved
in paternal care?

447

One study looked at the whole brain activation of Fos in male
and female biparental prairie voles exposed to either a pup, or to a
non-social olfactory stimulus (Kirkpatrick et al., 1994). Essentially,
they determined that pup exposure elicited the same Fos
expression in males and female prairie voles in the regions
examined such as the medial nucleus of the amygdala, medial
preoptic area, bed nucleus of the stria terminalis, and paraventricular nucleus of the hypothalamus (Kirkpatrick et al., 1994),
although this work was not looking at parental motivation per se.
Whether brain region activation of Fos is similar in males and
females of biparental species is yet to be determined, particularly
in the context of motivation.
The neuropeptides oxytocin and vasopressin work together
with olfactory information to mediate social memory in parental
and pair bonding relationships, a mechanism that may be of great
evolutionary advantage for fathers according to kin recognition
theory (Widding, 2007). In rodents, olfactory cues are conveyed to
brain regions that are also targeted by oxytocin and vasopressin,
like the medial amydgala and lateral septum via the vomeronasal
organ to modulate the formation of social memories (see Bielsky
and Young, 2004). The olfactory processes underlying social
memory appear to be crucial to offspring survival, and this is most
likely a result of the ensuing social memory that results from
paternal experience or even from social olfactory cues from
females. The latter instance can be seen in male Swiss-Webster
laboratory mice that kill their own young in the presence of an
unrelated female, but do not harm unfamiliar pups when paired
with a familiar female (Huck et al., 1982). When males of this
species are pre-exposed to the urine of an unfamiliar female
mouse before contact with her and her young, the rates of
infanticide diminish, pointing to the importance of olfactory cues
underlying the occurrence of infanticide and paternal behavior
(Huck et al., 1982). However, once infanticidal tendencies have
subsided, some rodent species will show parental behavior to all
pups, regardless of their genetic relation or familiarity with the
mother (Elwood and Ostermeyer, 1986). For example, male
gerbils will act parentally to both gerbil and mouse pups until
after their first litter is born. After this, parentally experienced
gerbils will be infanticidal toward mouse pups although they will
act parentally toward both related and unrelated gerbils (Elwood
and Ostermeyer, 1986).
The important role of the vomeronasal organ is demonstrated in
studies reporting that removal of this structure facilitates paternal
behavior in a subset of virgin males rats (n = 8; 50%), but most of all,
abalation of this structure significantly reduced infanticide
(Mennella and Moltz, 1988). Mennella and Moltz, 1988 proposed
that removal of the vomeronasal organ relieved the aversiveness of
the higher molecular weight odors emitted from the pups, and so
infanticide was reduced, while parental behavior occurred in some
cases.
It should be noted that inhibition of infanticide and paternal
behavior are not solely dependent on olfactory cues in some
species. For example, in a study using the male California mouse,
copulation and paired housing did not prevent infanticide in most
males. Parental behaviors were only initiated following 3 days
postpartum exposure to the female (Gubernick et al., 1994).
However, a small proportion of mice became paternal following
copulation and 24 h of cohabitation, behavior that continued
throughout pregnancy and into the postpartum period, regardless
of whether the female was present or absent from the litter
(Gubernick et al., 1994).
Still, in species where olfactory cues are critical to initiate mate
bonding, and/or attachments with infants (such as maternal ewe
and selective infant unions (see Bielsky and Young, 2004)) there
seems to be a motivational mechanism mediating the social
recognition process. Indeed, Young’s group has proposed that

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conditioned partner preference may result through the activation
of oxytocin and vasopressin pathways, alongside a corresponding
excitation of reward systems. Ultimately, this process may result in
the association of mate olfactory cues and reward associated with
the act of copulation, and therefore subsequent pair bond
formation (see Bielsky and Young, 2004). We might then expect
the same sort of selective social recognition/bonding toward
offspring to occur in prairie voles and other biparental species,
because of the presumed rewarding aspects of parenting. However,
this is not always the case. These animals will parent unrelated
offspring, which seems odd from a genetic propagation perspective, particularly since the mechanisms for such recognition/
discrimination are clearly in place for these monogomous pair
bonding species.
14. Further considerations
Any male can be a father. It takes someone special to be a dad.
Author Unknown
Animal models are developed in order to gain insight into the
neurobiological and behavioral basis of human actions and social
organization. In the case of paternal investment, which typically
occurs within a monogamous framework, only 3–5% of mammalian species are naturally paternal (Clutton-Brock, 1989). Among
the paternal models are tamarins (Ziegler et al., 2004), marmosets
(Almond et al., 2006), gerbils (Piovanotti and Viera, 2004), and
hamsters (Hume and Wynne-Edwards, 2005), in addition to the
dominant animal models, voles (Young et al., 1998) and mice
(Trainor and Marler, 2001). These species are used as a reference to
describe paternal care. However, the neurochemical and hormonal
activation between these models does not have a one-to-one
comparison across gestation and offspring development. For
example, low levels of vasopressin receptor density in the lateral
septum (which is implicated in paternal care) are common in
monogamous compared to polygamous voles (Wang, 1995; Wang
et al., 1997), but the opposite relationship in vasopressin density
has been reported between the paternal California mouse and the
nonpaternal white-footed mouse (Bester-Meredith et al., 1999).
This suggests that the pathways underlying paternal care evolved
differently.
15. Limitations of smaller animal models
The study of the contribution of males to paternal care
indicates that there are significant differences between humans
and animals. For example, some nonpaternal animals exposed to
stressful environmental or physical challenges such as changes to
ambient temperature or light (Parker and Lee, 2002) or forced
swim stress resulting in elevated corticosterone levels (Bales
et al., 2006) will commence facultative care. In human parents,
stressful situations (particularly economic and social stressors)
are more apt to lead to disturbances such as depression (Parke
et al., 2004; Areias et al., 1996) and/or negative behavior toward
children such as hostile parenting (Parke et al., 2004). In extreme
circumstances, this can include parental absence due to marital
conflict or longer working hours. The associated human stressors
are often chronic pressures (in the form of daily hassles) whereas
the stressors applied to animal species occur in the context of a
laboratory situation. Along this line, when housed in close
quarters with young, some mammals may demonstrate paternal
behaviors that do not normally occur in nature (see Woodroffe
and Vincent, 1994). Therefore, due to the limitations of animal
models, we must be cautious when employing them to study
paternal behavior.

16. Animal models of varying paternal structures
Human fathers are able to play, teach, punish, and provide for
children, and non-human primates can account for many of these
behaviors. For example, male Golden lion tamarins will participate
in carrying and socializing with infants (Sussman, 2000), in
addition to provisioning juveniles with novel food (Rapaport,
2006). It is known that Rhesus monkeys, one of the least paternal
primate species, will engage in male adult–infant play, in the
laboratory, following an initial familiarization period (Redican and
Mitchell, 1973). This type of play has been described as brief
episodes of ‘‘rough-play’’ including pinning, and restraining,
alongside more docile behaviors such as grooming (Redican and
Mitchell, 1973).
One approach is to determine ‘archetypes’ and corresponding
behavioral models in order to describe human paternal behavior
more fully. For example, the cooperative breeding systems of
meerkats (Brotherton et al., 2001; Clutton-Brock et al., 1998; Cant,
2003) and Golden lion tamarins (Sussman, 2000; Rapaport, 2006)
might be reasonable models of complex human parenting
relationships that include divorce and step-families. Even the
occurrence of same-sex parenting relationships may be accounted
for in the cooperative breeding system. In the animal kingdom,
there are diverse family structures that are as variable as the
human, culturally influenced, family system.
Infanticidal animal models might be compared to aggressive
and abusive parenting that is seen in both primate and rodent
models.
17. Common neural correlates
Ultimately, it is difficult to compare attachment and bonding
directly from animals to humans to describe parental care;
however some of what we have learned from animals does relate
back to Homo sapiens. Nonetheless, the relationship between
dopamine and regions of the brain related to reward do suggest a
semi-conserved motivational mechanism underlying attachment
(Insel, 2003; Bartels and Zeki, 2004; Bielsky and Young, 2004).
Thus, laboratories around the world are continuing their pursuit to
explore the intricacies of the brain regions associated with
attachment.
A fMRI study in humans compared previous findings of neural
activity associated with romantic love (see Bartels and Zeki, 2000)
to those of maternal love (Bartels and Zeki, 2004). In the human,
both romantic and maternal love activated the substantia-nigra
and globus pallidus, in addition to the bed nucleus of the stria
terminalis and ventral tegmental area, though the latter two
structures were reportedly too small to properly verify using the
fMRI technique. Unlike maternal love, romantic love was
associated with hippocampal and hypothalamic activation,
whereas maternal love was associated with an activated periaqueductal gray (Bartels and Zeki, 2004). The investigators
concluded that since these reward-related structures also contain
vasopressin and oxytocin receptors, the neural control of attachment is comparable in both humans and animals (Bartels and Zeki,
2004). In the case of romantic love, the authors did not observe sex
differences in terms of brain region activation (Bartels and Zeki,
2004). Because the brain activation associated with maternal love
and romantic love is similar, it may be that human maternal and
paternal love have similar neural correlates.
18. Conclusion
A large proportion of the animal literature focuses specifically
on the maternal aspect of parenting, while ignoring the contribution of the father. This is interesting given that the role of human

A.C. Kentner et al. / Neuroscience and Biobehavioral Reviews 34 (2010) 438–451

fathers is becoming more emphasized in the literature and, in fact,
many fathers report that they would like to be more involved with
their children (Milkie et al., 2004).
The early research in this area focused on male ‘maternal
behavior’ with a change in the 1990s toward a recognition of
‘paternal behavior’ and a more recent and ongoing development
toward the exploration of ‘parental behavior’. A recent shift in
societal norms related to issues of parenting has resulted in
reconsiderations of our labels and the relative importance of
paternal behavior. These conceptual changes have accompanied
and influenced our understanding and evaluation of parental care.
In the animal literature, paternal investment is necessary in
some models for the survival of the offspring. Fathers may
contribute differently from the mother, but they are still an
important support system to both the mother and offspring. The
same can be said of human fathers. In order to understand the full
contribution of fathers to the family unit, however it may be
composed, it is probably best to see how the unit functions
together as a symbiotic system (for example, Oliveras and Novak,
1986; Storey and Snow, 1987; Wynne-Edwards and Lisk, 1989;
Timonin and Wynne-Edwards, 2006, 2008; and various works by
Storey, see Storey et al., 2006), as opposed to determining paternal
behaviors in isolation from mothers, or other guardians, in both
human and animal studies.
It doesn’t matter who my father was; it matters who I remember he
was.
Anne Sexton
Acknowledgements
We would like to thank the Natural Sciences and Engineering
Research Council of Canada and the Alberta Heritage Foundation
for Medical Research for their kind support. In addition we would
like to thank our anonymous reviewers for their helpful comments
and suggestions.
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