reproduction in primate

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    Comparative aspects of reproduction inComparative aspects of reproduction in

    female primatesfemale primates

    Seasonality

    Ovarian cycles

    Pregnancy

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    Jan

    Feb

    Mar Ap

    rM

    ayJun

    Jul

    AugSe

    pOct

    Nov

    Dec

    0

    20

    40

    60

    80Annual distribution of birth (%)

    0

    5

    10

    15

    20

    25

    Most species exhibit some seasonal variation in timing of births

    HighHigh degreedegree ofof variationvariation -- fromfrom mild to extrememild to extreme

    SeasonalitySeasonality in Primatesin Primates

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    Taxonomic group Degree of seasonality

    Prosimians

    Malagasy +++Galagos/Iorises +++/++

    Tarsiers ++/??

    New World monkeys

    Callitrichidae ++/+Cebidae

    Saimiri ++

    Others (howlers) +/-

    Old World monkeys

    Cercopithecinae ++/+ (>20 from equator)+/- (

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    PrimatesGeographical distribution

    Prosimians

    Anthropoids

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    Seasonality: Causal factors

    1 Photoperiod

    Latitudinal gradients-rhesus/Japanese macaques-higher latitudes, more strictly

    seasonalLemurs-breeding onset at reduced photoperiod (very sensitive, ie 0.5h change)

    2 Rainfall and vegetation

    Expect to be important in equatorial regions where light (temperature)

    differences are minimal

    Wet season births (eg Saimiri and other Neo-tropicals)-linked to food

    abundance during weaning. Thus, nutrition one of the main influences

    3 Proximate causes

    If rainfall (food availability) coincides with births/weaning, what triggers onset of

    mating behaviour (and conception) 5-6 months earlier???

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    Reproductive Seasonality in Hanuman Langurs

    JanFebar

    Apr ay

    JunJ

    ulAugSepOctNovDec

    0

    5

    10

    15

    20

    25

    30

    Number

    Koenig et al., 1997

    Distribution of births

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    Hanuman Langurs: Faecal Progestin Profiles

    Proge

    stin

    (g/g)

    0

    5

    10

    15

    20

    June July August

    Conc

    Female O2

    Proge

    stin

    (g/g)

    0

    10

    20

    30

    40

    May June July Aug Sept Oct Nov

    Female O7

    Ov Ov Conc

    Ziegler et al, 2001

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    Onset of ovarian

    cycles

    A M J J A S O N

    A M J J A S O N

    Month of year

    Onset of ovarian

    cycles

    n = 7

    Rainfall Female condition

    Seasonal onset of ovarian cyclicity in relation to rainfall andbody condition in Hanuman langurs (Ramnagar)

    Ziegler et al, 2001

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    Ovarian cycles

    Oestrous cycle

    Term oestrus or heat refers to brief, restricted and intense period

    of sexual receptivity/urge

    Menstrual cycle

    Term menstruation, initially used for human female, refers to

    discharge of blood from uterus at approximately monthly intervals

    (Latin mensis=month). Absent in prosimians, most New Worldmonkeys

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    Ovulation

    Post-ovulatory

    Luteal or

    secretory phase

    Pre-ovulatory

    Follicular or

    proliferative phase

    Component phases of the primate ovarian cycle

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    Gonadotrophin (LH

    and FSH) and steroid

    hormone (E2 and P)

    profiles during theprimate ovarian cycle.

    Hormone levels and

    timing of events are

    based on the humancycle

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    Monitoring the menstrual cycle

    Alan McNei lly

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    Endocrine changes in menstrual cycle

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    Ovarian cycle

    - repetitive expression of Hypothalamic-Pituitary-Ovarian axis, with

    associated structural and functional changes in target tissues of the

    reproductive tract

    Brain-pituitary-ovary-uterus/oviduct

    Behaviour-mating

    Gamete-release mature egg

    Reproductive tract-fertilization and implantation

    Co-ordination of events at multiple levels:

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    Control mechanisms

    Pulsatile secretion of gonadotrophins

    Feedback mechanisms Follicle selection

    Ovary is Zeitgeber

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    Pulsatile LH secretion and the menstrual cycle

    Follicular Luteal

    LH pulse frequency 1 per h 1 per 4h

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    The GnRH pulse generator

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    When the follicle is ready to ovulate, estradiol triggers a

    surge release of GnRH switching LH secretion switches

    from pulsatile to surge type

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    The ovary is Zeitgeber

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    Menstrual cycle characteristics in thelowland gorilla

    26 - 3930.4 1.5Total cycle (days)

    12 - 1514.0 0.4Luteal phase (days)

    12 - 2416.4 1.5Follicular phase (days)

    RangeMean s.e.m.

    (From Czekala et al., 1988)

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    Relative standard deviation of luteal

    phase length

    0

    1

    2

    3

    4

    5

    6

    Freque

    ncy

    1.0

    (S.D. luteal phase / S.D. follicular phase)

    (16 species)

    From van Schaik, Hodges and Nunn, 2002

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    Total cycle Follicular phase Luteal phase

    Radiation

    Prosimians

    New World

    Old World

    ANOVA:

    Post-hoc:

    N x SD

    19 33.77 7.91

    20 20.03 5.84

    38 31.01 3.67

    N x SD

    3 7.33 4.04

    8 6.90 2.15

    22 14.99 3.37

    N x SD

    4 26.38 1.78

    8 13.54 4.83

    21 14.94 1.58

    F[2,74]=35.71***

    Pla

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    Mating periods within the ovarian cycle of primates

    3-18

    3-12

    Cercopithecoidea- Cercopithecinae

    - Colobinae

    4-15Hominoidea

    5-12

    2-8

    Ceboidea

    - Callitrichidae

    - Cebidae

    1Tarsoidea

    1-2Lorisoidea

    1-3Lemuroidea

    Median mating period

    (range)

    Superfamily/Family

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    Why extend the receptive period?

    multiple mating partners possible

    male monopolization more difficult

    To promote promiscuity

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    IncreasedIncreased promiscuitypromiscuity isis linkedlinked to ato a femalefemale strategystrategytoto protectprotect herher ownown reproductivereproductive interestsinterests

    improved group defense, reduced predation risk

    increased paternal carereduced risk of infanticide

    increased genetic diversity

    reduced risk of fertilization with low quality sperm

    potential for female to influence paternity outcome

    Help maximize female reproductive output; quality vs quantity

    Potential benefits include:

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    Why extend the receptive period?

    multiple mating partners possible

    male monopolization more difficult

    To promote promiscuity

    Requires that timing of ovulation is unpredictable

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    Hanuman Langurs: Receptive Periods and Timing of Ovulation

    Receptive periods

    Number of ovulations

    days relative to ovulation

    -12 -10 -8 -6 -4 -2 0 2 4 6 8 10 12

    **

    **

    *

    *

    **

    *= conception cycles

    % of receptive period

    0-20 21-40 41-60 61-80 81-100

    From Heistermann et al, 2001

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    0

    510

    15

    20

    25

    0

    10

    20

    30

    40

    -8 -6 -4 -2 0 2 4 6

    0.0

    0.8

    1.6

    2.4

    Days from ovulation

    Female solicitations

    Copulations

    Copulations persolicitation

    Sexual behaviour in relation to time of ovulation

    %o

    ftotal

    %o

    ftotal

    N

    umber

    From Heistermann et al, 2001

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    Male rank

    1 2 3 extra-group

    %C

    opulatio

    ns

    Numberofinfants

    Male rank, copulations and paternity outcomein Hanuman langurs

    0

    10

    20

    3040

    50

    60

    0

    1

    2

    3

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    PregnancyPregnancy

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    cl formation cl regression

    Ovulation

    129630

    P (non-fertile)

    P (fertile)

    CG

    Implantation

    Window cl rescue

    15

    Maternal recognition of pregnancy corpus luteum rescue

    Luteo-

    placental

    shift

    30-40

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    Total cycle Follicular phase Luteal phase

    Radiation

    Prosimians

    New World

    Old World

    ANOVA:

    Post-hoc:

    N x SD

    19 33.77 7.91

    20 20.03 5.84

    38 31.01 3.67

    N x SD

    3 7.33 4.04

    8 6.90 2.15

    22 14.99 3.37

    N x SD

    4 26.38 1.78

    8 13.54 2.33

    21 14.94 1.58

    F[2,74]=35.71***

    Pla

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    Significance of extended luteal phasein Prosimians

    at 28 days, luteal phase approaches timing of onset

    of luteo-placental shift in Anthropoid primates

    endocrine response to conception is minimal

    no detectable chorionic gonadotrophin; gene for CG absent

    no corpus luteum rescue comparable to that seen in

    Anthropoid primates

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    Total cycle Follicular phase Luteal phase

    Radiation

    Prosimians

    New World

    Old World

    ANOVA:

    Post-hoc:

    N x SD

    19 33.77 7.91

    20 20.03 5.84

    38 31.01 3.67

    N x SD

    3 7.33 4.04

    8 6.90 2.15

    22 14.99 3.37

    N x SD

    4 26.38 1.78

    8 13.54 2.33

    21 14.94 1.58

    F[2,74]=35.71***

    Pla

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    cl formation cl regression

    Ovulation

    129630

    P (non-fertile)

    P (fertile)

    CG

    Implantation

    Window cl rescue

    15

    Maternal recognition of pregnancy corpus luteum rescue

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    Timing of Key Events Occurring During Early Pregnancy in Primates

    Species Gestation *Embryo *CG first *Luteo-

    length attachment detected placental(days) shift

    Marmoset

    Rhesus

    Baboon

    Chimpanzee

    Human

    * approximate days after ovulation

    144

    168

    184

    235

    280

    10-11

    8-10

    8-10

    7-8

    7-8

    13

    12

    12

    11

    10

    40-60

    20-25

    20-30

    ?

    40-50

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    Relationship between gestation length and maternal

    body weight in primates

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    Deviation from expected gestation length in Callitrichid monkeys

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    Schematic diagramme of the main hormonal changes

    during human pregnancy

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    Progesterone

    Oestrone (E1)

    Oestriol (E3)

    O E i d i P i L

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    Oestrogen Excretion during Pregnancy in Lemurs

    Eulemur coronatus

    Estrogen Excretion during Pregnancy in Lemurs

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    Estrogen Excretion during Pregnancy in Lemurs

    -130

    -120

    -110

    -100-9

    0-8

    0-7

    0-6

    0-5

    0-4

    0-3

    0-2

    0-1

    0 0 10 20 30

    0

    1

    2

    3

    4

    5

    6

    Col 1 vs Elba-Eges

    -130

    -120

    -110

    -100-9

    0-8

    0-7

    0-6

    0-5

    0-4

    0-3

    0-2

    0-1

    0 0 10 20 30

    0

    1

    2

    3

    4

    5

    6

    Male fetus

    Female fetus

    C

    C

    Days before and after birth

    Days before and after birth

    Et

    (

    g/g

    fae

    ces)

    Et

    (

    g/g

    fa

    ece

    s)

    Individual profiles

    Lack of early gestational

    estrogen rise

    Estrogen production dependent onfetal sex

    0

    5

    10

    15

    20

    25

    E. rubriventer

    E. flavifrons

    E. coronatus

    H. griseus

    Relation to sex of fetus

    Et

    (

    g/g

    fa

    ece

    s)

    M F

    Primates

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    Primates

    Highly successful, widespread and diverse

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    .the end

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    Field Endocrinology

    Combines laboratory and field-based methodologies

    Contributes to more integrated approach

    Ecology

    Genetics BehaviourPhysiology

    Infectious diseases

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