Male Behavioral Response to Infant-Stimuli:
The Role of Fatherhood and Hormones
Do hormones and social experience affect
the intensity of response to infant cries?
Common Marmosets
(Callithrix jacchus)
Bi-parental
Cooperative Breeders
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•
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Fathers and mothers both provide parental care
Other group members help raise infants
Nursing, Grooming, Protection, Thermoregulation
Carrying and Transportation in Arboreal Habitat
Cooperatively Breeding and
Bi-parental Species:
Social Environment
•Learning skills for future
•Physiology, bonding, health
Access to Resources
Shared Expenses
•Infant care
•Group defense
•Foraging
© E Heymann
Adult moustached tamarin with twins:
Saguinus mystax
© M Eberle
Mouse lemur: Microcebus murinus
Retrieval and Carrying
© CY Boe
Cottontop tamarin
infant transfer:
Saguinus oedipus
Societal and
economic factors
influence the
roles that fathers
play in their
families.
Human father involvement is associated with positive
cognitive, developmental, and social outcomes such as:
•improved weight gain in preterm infants
•improved breastfeeding rates
•higher receptive language skills
•higher academic achievement Garfield & Isacco, Pediatrics, 2006
What proximate mechanisms
maintain fathers’ involvement
in infant-caretaking?
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The Marmoset Model
Male Life Phases
Natal
Parents, siblings
Hormones - Puberty
Alloparenting skills
Males develop
Paired
• Mate
• Pair-bonding Behavior
• (OT)
Father
•
•
•
•
Mate, offspring
Hormones – Pregnancy
Hormones – Infants
Paternal skills
How do social species coordinate their behavior with the appropriate social
environment? What physiological (or other) mechanisms make it possible?
For example, for activities like infant-care?
Fatherhood Affects Hormones
Hormonal changes in expectant fathers
(during pregnancy)
Estradiol
Estradiol ng/ml
2.5
2.0
1.5
1.0
0.5
0.0
month 2
month 3
month 4
month 5
Prolactin
Prolactin ng/ml
4
3
2
1
0
month 2
month 3
month 4
pregnancy month
month 5
Ziegler et al., 2008 Royal Soc Biol. Let. 2:181-183.
Hormonal changes after infants are
born (during care-taking)
Testosterone decreases
Prolactin increases
Hormonal changes after infants are
born (during care-taking)
Prolactin levels elevate
during infant care
Ziegler et al., 2009. Horm Behav 56:436-443
Dependency and age of infants
influence hormones (scent cues).
Weaning starts 6wks – ends 12wks.
12 weeks: Ziegler et al. 2011
Ziegler et al., 2011 Horm Behav 59:265-270
Example Hormone Timeline
Start
Wean
Prolactin
Testosterone
Estrogen
6wk
Wean
Complete
Birth
12wk
1
2
3
4
5
6
7
8
9
10
11
12
Fathers have different
hormonal fluctuations
than nonfathers.
Fathers’ hormones change:
•During pregnancy
•With presence of infants
•According to age of infants
Social
Physiology
“Social Behavioral Neuroendocrinolgy”
What is it? How does it work?
Sensory Stimuli
Olfactory
Auditory
Visual
Touch
Taste
CNS stimulation
neurochemistry
endocrine
system
behavior
Fatherhood Affects Behavioral
Responsiveness to Infants
Marmosets are very responsive to
sensory stimuli. All the senses are used
for social communication.
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•
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•
Scent
Auditory
Infant distress calls “Help!”
Visual
Contact/touch
Taste
What is this little fellow doing?
Testing variation in fathers’
responsiveness to infant stimuli
Infant
distress
call
1. Live infant
familiar
unfamiliar
2. Infant stimuli
familiar
unfamiliar
Fathers responded significantly
more to recorded calls
than did nonfathers
Infant directed behaviors
•Look at infant
•Enter stimulus cage
•Touch
•Sniff
•Face lick
•Anogenital lick
•Attempt to retrieve stimulus
Stimulus directed behaviors
•Look at stimulus
•Enter bridge obstacle
•Enter stimulus cage
•Investigate for source of cries
•Manipulate stimulus
•Attempt to retrieve stimulus
Zahed et al., Am J Primatol. 70:84-92, 2008
Fathers responded more quickly to
infant stimuli than did nonfathers.
Zahed et al., Am J Primatol. 70:84-92, 2008
How does the social experience of being
present for pregnancy and own offspring
affect an adult male’s responsiveness to
communication from the infant?
social
behavior
social
hormones
social
?hormone
s
behavior
NEW STUDY
Both fathers and nonfathers are capable of infant-caretaking.
We know that 1) fatherhood affects hormones and 2) fathering
experience affects responsiveness to infant cues.
Do changes in hormones affect
parenting behavior?
Do hormonal fluctuations have a
different effect for males in two
different life phases: with and
without offspring?
STUDY DESIGN
Hormone Treatment
Acoustic Stimulus Test
•Testosterone
•Estrogen
•Contol (Oil Vehicle)
Home Cage
Stimulus Cage
Behavior: “Enter Bridge”
Study Phases for Each Subject Male
1st Hormone:
Habituate
(30min)
2nd
Hormone:
rd Hormone:
3
Sample (10min)
Sample (10min)
Habituate
(30min)
Sample (10min)
2-4 days
Injection
Stimulus (v/c)
Stimulus (v/c)
Behaviors Sampled
A
B
C
D
E
F
G
H
I
J
K
L
M
Attempt Retrieve Stimulus Device (Never Occurred)
Look at Stimulus Cage
Manipulate Stimulus Device (Never Occurred)
Enter Stimulus Cage
Chatter Vocals
Long Call Vocals
Look Out of Cage
Enter Home Cage
Enter Bridge
Investigate/Search Home Nest-Box
Look at Stimulus Device
Enter Home Nest-Box
Investigate/Search Stimulus Nest-Box
Behaviors Sampled
Most Direct Interpretation as “Infant Stimulated Motivation”:
A
C
D
I
M
Attempt Retrieve Stimulus Device (Never Occurred)
Manipulate Stimulus Device (Never Occurred)
Enter Stimulus Cage**
Enter Bridge**
Investigate/Search Stimulus Nest-Box
Challenges in Interpreting Frequency:
B
K
H
J
L
Look at Stimulus Cage
Look at Stimulus Device
Enter Home Cage
Investigate/Search Home Nest-Box
Enter Home Nest-Box
Addressing Individual Variation or Negative Responses (e.g. T):
E
F
G
Chatter Vocals
Long Call Vocals
Look Out of Cage
CHALLENGES WITH PRIMATES:
Characteristics of Primate Social groups
– Variation in demographics influences reproduction,
social behavior, cognition, learning opportunities. Often,
this variability, and the response to it, is exactly what
“makes them primates”. We need to balance control of
variables with letting them live their lives. Don’t want to
control away their “primate-ness”, which is what we’re
trying to learn about. (Experience. An art.)
– Variation among individuals – sometimes very high.
– Low numbers of subjects and groups, long life-spans.
(N, sharing study subjects)
– Things sometimes don’t go according to plans (e.g.
sampling days, pregnancy, numbers of infants).
Thank you for your help!
END TALK
ADDTL BACKGROUND
The Marmoset Model
Males carry and care for
infants directly after birth
High variability between
males in their infant care
behaviors
High reproductive
output:
Multiple infants
5 month gestation
Postpartum conception
Infant carrying
lowers father’s weight
420
410
*
Weight in grams
400
390
380
370
Prepartum
Week 1
Week 2
Post partum weeks
Week 3
Parental Experience Affects
Responsiveness
• Recorded calls had almost as much
valance as live infants
• Fathers showed the largest response
• Fathers varied individually
Odor cues have valance and influence the social bonds
in cooperative breeding species which may protect
the integrity of the group
Testosterone
Cortisol
Ziegler, Schultz-Darken, Scott, Snowdon, Ferris, 2005
Father variation in response
to infant stimuli
Response Frequency of Infant
directed behaviors
Frequency of behaviors
250
200
150
100
50
0
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15
Experienced father marmosets
Zahed et al., Am J Primatol. 70:84-92, 2008
Interpretation and the future
• Fathers are highly tuned into their social
environment – keeping them in a hormonal
flux
• Males are hormonally and behaviorally
responsive to social stimuli dependent
upon paternal experience