Stages of MaternalOffspring interactions

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• Stages of Maternal-Offspring interactions
• Conception, menstruation and early survival of
  the embryo
• Invasion of the placenta
• Maternal-fetal food fights
• (a) Glucose concentration
• (b) Blood supply
• Gestation length
• Survival of the fattest and cutest
• Sucking, crying, whining, weaning
• Survival and increased reproduction of the
  slower-developing child

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Maternal-fetal interactions over resources during
gestation replaced by maternal-child interactions
over resources during lactation
period Gestational interactions are
biochemical After birth, interactions are also
behavioral suckling and crying can be seen as
forms of begging behavior PLACENTA-gtBREAST In
public health literature, interests of mother
and young child are seen as
fully coincident Main health concerns in
gestation fertility, miscarriage, growth
restriction, pre-eclampsia, gestational
diabetes Main health concerns in lactation
period failure to thrive, infant obesity, colic
difficulty in establishing postnatal nutrition is
one of main reasons that new mothers visit family
doctor
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• SUCKLING KEY CONSIDERATIONS (JK Wells, 2002)
• The lactational infant growth period is the only
  time after birth when growth is regulated (and
  limited) by food intake - later, it is regulated
  hormonally
• Early growth is an important determinant of
  survival in childhood and adult size, which is
  positively associated with fitness
• Suckling, especially at night and especially in
  nutritionally-stressed mothers, causes
  lactational amenorrhea (natural contraception,
  due to high prolactin)
• Suckling itself is not energetically expensive
  for children, but for mothers it is much more
  expensive than gestation (up to 30 of daily
  energy, vs 10 for gestation). Costs of lactation
  are alleviated via maternal fat stores and
  complementary foods
• Mothers put benzodiazepine-like sedatives in
  breast milk, which suggests a strategy of mothers
  to constrain suckling
• Optimal time of weaning for mother is earlier
  than optimal time for child in some primates,
  intense suckling near weaning, but mother
  withholds nipple more -gt weaning conflict, also
  found in humans

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Mother controls Infant controls -access to
nipple -crying frequency,intensity -content of
breast milk -attempted suckling -lactational
amenorrhea system -suckling intensity,
duration -threshold of response to crying
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• INFANT CRYING KEY CONSIDERATIONS (JK Wells,
  2002)
• Crying is energetically costly (metabolic rate
  20x higher
• than in quiet sleep, and it is a graded signal
  (continuously adjustable)
• (2) Crying occurs in context of hunger, pain,
  fear, vocalization
• and language, and separation - mainly separation
  in non-human
• primates, mainly hunger in humans
• (3) Crying and intake peak during highest-growth
  stage (6 weeks)
• Six weeks 40 of energy intake to growth
• Three months 30
• Six months 10
• One year 5
• (4) Crying thus appears to usually
• serve as a (costly) more-or-less honest
• signal of need

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• Genetic and epigenetic evidence for
  mother-offspring
• conflict over suckling
• Mouse knockouts of several paternally-expressed
  imprinted
• genes (PEG3, GNASxl) exhibit severely-impaired
  suckling
• behavior, due to hypothalamic and orofacial
  muscle defects
• (2) In humans, Silver-Russell syndrome (due to
• biases towards maternal-gene expression) involves
  
• impaired orofacial muscle development that
  interferes
• with suckling and other feeding
• In humans, Angelman syndrome involves increased
• suckling attempts, Prader-Willi syndrome involves
  decreased
• suckling attempts

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Oppositely-imprinted neurogenomic disorders
Prader-Willi Angelmansyndromes

• Angelman maternal deletion of 15q11-q13 or
  paternal UPD15 or UBE3A mutation

• Prader-Willi paternal deletion of 15q11-q13
  or maternal UPD15

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Angelman Prader-Willi

• prolonged suckling
• frequent crying
• hyper-active/sleepless
• picky about food after weaning in many cases

• poor suckling
• weak crying
• inactive/sleepy
• after weaning, develop hyperphagia, forage on own
  unselectively

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• INFANT CRYING A SIMPLE VERBAL MODEL (JK Wells,
  2002)
• -Initially, crying signals need
• -When provisioning is generous, needs inflate
  into wants
• -When provisioning is poor, crying level should
  reduce, to
• conserve energy
• -Maternal and offspring strategies are assumed to
  have evolved under
• resource limitation and no artificial
  contraception - infant is selected in context
• of sibling competition, mother in context of
  optimal investment in multiple
• offspring
• -Recent changes, resulting in mismatches between
  ancestral and current
• environments
• High resource levels in developed and some
  developing countries, may
• alter behavior of infant
• (2) Altered social environment, may alter
  maternal receptivity to
• signalling, or interpretation of signal

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Maternal response threshold (responsiveness to
given level of crying persistence in
fostering suckling
Offspring demand (levels of crying, attempted
suckling)
Dynamically-balanced tug of war
Usual situation,as in gestation
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Maternal response threshold (responsiveness to
given level of crying persistence in
fostering suckling
Offspring demand (levels of crying, attempted
suckling)
Dynamically-balanced tug of war OR Demand high
and/or response threshold low OR Demand low
and/or response threshold high
Usual situation,as in gestation Overnutrition U
ndernutrition
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• Implications of mismatches for health and
  disease, in context
• of mother-infant confluence and conflict of
  interest
• Overnutrition and early-onset obesity
• -medical criteria is centiles of weight adjusted
  for length
• -evolutionary criteria is offspring gaining more
  resources than
• optimal for mother to give, to point of
  maladaptation for both
• Increased transfer of resources to offspring
  predicted under
• increased offspring demand intensity TRUE, when
  resources are
• abundant fitness cost of signaling is lower
  mothers also give food and
• drink to resolve distress -gt crying develops
  into blackmail
• (b) lower threshold of response TRUE, changes in
  parental attitudes, style
• (c) cost of resource decreases TRUE, energy is
  no longer limiting, energetic
• tradeoffs are absent
• Also, (d) formula now has a higher energy density
  than breast milk, and

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• Implications of mismatches for health and
  disease, in context
• of mother-infant confluence and conflict of
  interest
• (2) Undernutrition and failure to thrive
• -medical criteria is centiles of weight adjusted
  for length
• -evolutionary criteria is offspring gaining less
  resources than
• optimal for mother or child
• Decreased successful food transfer to child, due
  to some combination of
• reduced demand by child, increased response
  threshold by mother
• -Found in some neurodevelopmental disorders
  (Prader-Willi, Silver-Russell)
• but these are rare
• -Appears commonly due to subtle oral-motor
  dysfunction in child, and/or
• psycho-social factors in mother
• -Low levels of demand (crying, soliciting suck)
  can jeopardize milk supply

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Maternal response threshold (responsiveness to
given level of crying persistence in
fostering suckling
Offspring demand (levels of crying, attempted
suckling)
Dynamically-balanced tug of war OR Demand high
and/or response threshold low OR Demand low
and/or response threshold high
Usual situation,as in gestation Overnutrition U
ndernutrition
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• Implications of mismatches for health and
  disease, in context
• of mother-infant confluence and conflict of
  interest
• (3) COLIC - excess, inconsolable crying
• of unknown cause
• Often attributed to gastrointestinal pain,
• but no good evidence for this
• May be associated with crying as a signal of
  infant health and vigor,
• when such crying is energetically-affordable -gt
  colicky infants
• do not show reduced growth, but otherwise few
  tests, little evidence
• May be started or exacerbated by initial
  misinterpretation of signaling
• (is evidence for maternal-infant behavioral
  disruptions with colic)

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-Maternal response threshold (responsiveness to
given level of crying persistence in
fostering suckling Maternal-offspring
communication dysregulated
-Offspring demand (levels of crying, attempted
suckling) Offspring demand, vigor signals
dysregulated, high
Dynamically-balanced tug of war OR Demand high
and/or response threshold low OR Demand low
and/or response threshold high OR Demand, vigor
high, response threshold high or dysregulated
Usual situation,as in gestation Overnutrition U
ndernutrition COLIC
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CONCLUSIONS INFANT CRYING, FEEDING,
LACTATION (1) Problems with infant feeding seen
as physiological may be mainly behavioral, and
are usefully understood in terms of evolved
mother-offspring interactions involving mix of
cooperation of conflict, and mismatches to
ancestral environments (2) There is a direct and
close analogy between feeding during gestation,
and feeding during lactation, in that both
apparently involve evolved tugs-of-war between
mother and offspring (3) Disruption in these
tugs-of-war can help explain some of the major
public health problems associated with infant
feeding (4) Further tests based on functional
design and the comparative method are urgently
needed

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• Sucking, crying, whining, WEANING
• WEANING KEY CONSIDERATIONS
• Defined as beginning of food supplemental to
  breast-feeding,
• ending with cessation of breastfeeding
• Humans wean their children considerably earlier
  in the life course
• (3 years) than do other apes (5-7 years)
  the age of weaning is highly variable within and
  between cultures humans are only primate that
  weans offspring before they can forage
  independently interbirth intervals are very
  short in humans, for primates
• huge effects on human demography. Figure-gt
• Weaning marks a shift to allo-caregiver support
  (not independence)
• (4) Period just after weaning (usually due to
  birth of sibling) involves spike in mortality of
  weaned child, in traditional societies
  interbirth interval and child mortality are
  highly correlated in traditional societies
• (5) Appropriate weaning practices have huge
  effects on human health and well-being in
  developed and developing countries

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HUMAN
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Nutrition-related life-history stages for a
generalized mammal
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Evolution of human child feeding compared to
other mammals, primates
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Transitional flexible complementary feeding
appear unique to humans
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• Current international recommendations for optimal
  growth and development of healthy humans in
  favorable environment
• (1) start breastfeeding within one hour of birth
• (2) exclusive breast-feeding for six months,
  followed by nutrient-dense pathogen-free foods
• (3) gradual introduction of high-quality family
  food, with continued breast-feeding into the
  third year
• In reality, young child feeding practices are
  clinically suboptimal for most children and their
  mothers
• Why? A few reasons for the mismatch
• Infant formula availability (overnutrition, no
  immunological or other trace-nutrient
  components), loss of extended-family support,
  economically-curtailed breastfeeding,
  dysregulation of mother-offspring conflicts

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Commonly-observed pattern, not optimal for child
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Good Bad
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ROLE OF MOTHER-OFFSPRING CONFLICT IN WEANING
Time course of parent-offspring conflict over
parental investment
Both benefit Child benefits Both
suffer costs Costs on mother As child
ages and grows, benefits of breast-feeding to
child and mother decline, and costs to mother
increase, in terms of her investment in other
offspring Mother prefers to wean child earlier
than child prefers to be weaned
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Supports and constraints (trade-offs) on
breast-feeding vary among human cultures
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The balance of supports and constraints
influences when supplemental foods are introduced
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One example of how the conflict plays out, with
early supplementation
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When supplementation occurs before conflict
period, both mother and child suffer reduced
fitness, from high infant morbidity and mortality
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Who controls the timing, duration of weaning, and
how? Mothers control access to the breast and
supplementary food presentation, subject to
tradeoffs and constraints Offspring control
their behaviour tantrums, whining, and
persistence over breastfeeding and acceptance of
supplementary foods, or regression (acting
younger than actual age) - psychological
warfare (Trivers 1972) Mothers hold the
balance of power regarding cessation of
breastfeeding, and introduction of supplementary
foods
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Prader-Willi syndrome and the evolution of
human childhood (Haig and Wharton 2003)
-before usual age of weaning (2 or 3) weak muscle
tone, poor suckling, weak crying -after weaning,
develop hyperphagia, forage on own, highly
unselectively May reflect exposure of historical
genomic conflict over nature and timing of child
feeding -gt Prader-Willi baby is ideal in terms
of low energetic costs imposed on mother
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• Stages of Maternal-Offspring interactions
• Conception, menstruation and early survival of
  the embryo
• Invasion of the placenta
• Maternal-fetal food fights
• (a) Glucose concentration
• (b) Blood supply
• Gestation length
• Survival of the fattest and cutest
• Sucking, crying, weaning, whining
• Human childhood growth survival and increased
  reproduction of the slower-developing child

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• KEY CONSIDERATIONS Human growth patterns,
  compared to other primates
• Humans evolved from (precocial) primates, but
  have evolved to be altricial (relatively helpless
  and dependent, physically)
• (2) Human grow very quickly in the first year,
  especially in brain size (maintain high fetal
  rate) infant growth is nutrient-regulated -
  reduce vulnerable period
• (3) Humans grow very slowly between age 2 and
  puberty
• childhood growth is hormonally-regulated - they
  are staying young on purpose, with a big brain.
  Then comes the adolescent growth spurt
• (4) Long, extended lifespan, with slow aging
• (5) Menopause

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• Why do human children develop so slowly,
  physically, from
• weaning until reproductive maturity?
• Selective advantage from increased parental
  investment,
• in competitive environment
• (2) Key role of brain development and maturation
  in
• childhood - development of language motor
  skills, gaining
• cultural knowledge
• (3) Extrinsic mortality is low after infancy
• and weaning, so it is relatively safe to
• develop slowly (costs are low)
• MISMATCH Secular trend towards
• earlier age of menarche in girls due to
• recent enhanced nutrition (especially fat),
• results in shortening of childhood stage,
• asynchrony of brain body development

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• Stages of human life history
• Gestation
• Childhood
• (3) Reproductive period
• (4) Post-reproductive period
• GROWTH, MAINTENANCE AND REPRODUCTION ARE
• SUBJECT TO TRADE-OFFS
• TO ANALYZE SUCH TRADE-OFFS, WE USE
• LIFE-HISTORY THEORY

GROWTH and maintenance REPRODUCTION and
maintenance MAINTENANCE and allo- parental care