stages of maternal-offspring interactions (1)conception, menstruation and early survival of the...

Stages of Maternal-Offspring interactions

(1) Conception, menstruation and early survival of the embryo

(2) Invasion of the placenta(3) Maternal-fetal food fights

(a) Glucose concentration(b) Blood supply

(4) Gestation length(5) Survival of the fattest and cutest

(6) Sucking, crying, whining, weaning

(7) Survival and increased reproduction of the slower-developing child

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->BREAST

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

Expensive!

SUCKLING: KEY CONSIDERATIONS (JK Wells, 2002)

(1) 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

(2) Early growth is an important determinant of survival in childhood and adult size, which is positively associated with fitness

(3) Suckling, especially at night and especially in nutritionally-stressed mothers, causes lactational amenorrhea (natural contraception, due to high prolactin)

(4) 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

(5) Mothers put benzodiazepine-like sedatives in breast milk, which suggests a strategy of mothers to constrain suckling

(6) 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 -> weaning conflict, also found in humans

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

INFANT CRYING: KEY CONSIDERATIONS (JK Wells, 2002)

(1) 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, vocalizationand language, and separation - mainly separation in non-humanprimates, mainly hunger in humans

(3) Crying and intake peak during highest-growth stage (~6 weeks)Six weeks: 40% of energy intake to growthThree 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

(5) Crying may also serve as a signal of infant vigor, quality, to some degree

(6) Near weaning, crying shifts to become more nocturnal FUNCTIONAL DESIGN

Genetic and epigenetic evidence for mother-offspring conflict over suckling

(1) Mouse knockouts of several paternally-expressed imprintedgenes (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

Oppositely-imprinted neurogenomic disorders: Prader-Willi & Angelman

syndromes

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

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

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

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 currentenvironments

(1) 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

Offspring demand(levels of crying, attempted suckling)

Maternal responsethreshold (responsivenessto given level of crying; persistence in fosteringsuckling

Dynamically-balanced‘tug of war’

Usual situation,asin gestation



Dynamically-balancedtug of warORDemand high and/orresponse threshold lowORDemand low and/orresponse threshold high


Overnutrition

Undernutrition

Implications of mismatches for health and disease, in context of mother-infant confluence and conflict of interest

(1) 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:

(a) increased offspring demand intensity: TRUE, when resources are abundant fitness cost of signaling is lower; mothers also give food and drink to resolve distress -> 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 with formula intake is not constrained by maternal production


(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-Weak suckling also reduces efficiency of bottle-feeding-Signaling (crying) by baby develops to be cost-ineffective (as in famine)-Parents may not recognize feeding difficulties, lack reference information-Hospitalization does not address root cause - behavioral intervention more effective



Dynamically-balancedtug of warORDemand high and/orresponse threshold lowORDemand low and/orresponse threshold high


Overnutrition

Undernutrition


(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 -> colicky infantsdo 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)

-Offspring demand(levels of crying, attempted suckling)Offspring demand, vigor signals dysregulated, high

-Maternal responsethreshold (responsivenessto given level of crying; persistence in fosteringsucklingMaternal-offspring communication dysregulated

Dynamically-balancedtug of warOR

Demand high and/orresponse threshold lowOR

Demand low and/orresponse threshold highOR

Demand, vigor high, response threshold highor dysregulated


Overnutrition

Undernutrition

COLIC

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

Sucking, crying, whining, WEANINGWEANING: KEY CONSIDERATIONS

(1) Defined as beginning of food supplemental to breast-feeding, ending with cessation of breastfeeding

(2) 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->

• 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

Nutrition-related life-history stages for a generalized mammal

Evolution of human child feeding compared to other mammals, primates

Transitional & flexible complementary feeding appear unique to humans

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

Commonly-observed pattern, not optimal for child

Good

Bad

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

Supports and constraints (trade-offs) on breast-feedingvary among human cultures

The balance of supports and constraints influences when supplemental foods are introduced

One example of how the conflict plays out, with early supplementation

When supplementation occurs before conflict period, both mother and child suffer reduced fitness, from high infant morbidity and mortality

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

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 historical genomic conflict over nature and timing of child feeding -> Prader-Willi baby is ‘ideal’ in terms of low energetic costs imposed on mother

Stages of Maternal-Offspring interactions

(1) Conception, menstruation and early survival of the embryo

(2) Invasion of the placenta(3) Maternal-fetal food fights

(a) Glucose concentration(b) Blood supply

(4) Gestation length(5) Survival of the fattest and cutest(6) Sucking, crying, weaning, whining

(7) Human childhood growth: survival and increased reproduction of the slower-developing child

KEY CONSIDERATIONS: Human growth patterns, compared to other primates

(1) 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

Why do human children develop so slowly, physically, from weaning until reproductive maturity?

(1) Selective advantage from increased parental investment, in competitive environment

(2) Key role of brain development and maturation in childhood - development of language & motor skills, gainingcultural 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

Stages of human life history

(1) Gestation(2) 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

stages of maternal-offspring interactions (1)conception, menstruation and early survival of the...

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