Development and Life Span - Primate Behavior Lecture

03/20/2025 DEVELOPMENT AND LIFE SPAN 1 1  03/20/2025 THE PRIMATE LIFE CYCLE 3 2  03/20/2025 Outline Lifespan and Life expectancy...

03/20/2025 DEVELOPMENT AND LIFE SPAN 1 1  03/20/2025 THE PRIMATE LIFE CYCLE 3 2  03/20/2025 Outline Lifespan and Life expectancy Socialization & infant care – Mothering – Adult male-infant interactions – Allomothering (or alloparenting) – Peers Puberty & the transition to adulthood Adulthood & ageing Menopause 4 3  03/20/2025 Life expectancy vs Life Span Life expectancy: an average computed over all people including those who die shortly after birth, those who die in childbirth, in early adulthood, in wars, and those who live unimpeded until old age Lifespan: an individual-specific concept and maximum lifespan is an upper bound rather than an average 5 4  03/20/2025 Primate Lifespans “Contrasted to most other mammals, primates have long average adult lifespans [i.e., live longer] and few babies per year for their adult body size.” –Charnov & Berrigan (2005) 6 5  03/20/2025 Life history model 7 6  03/20/2025 Primate Lifespans Lifespan and body size correlated – larger bodied animals (including primates) live longer Monkeys live 15 – 30 years Great apes live up to 50 years Humans can live up to 120 years 8 7  03/20/2025 Male vs. Female Lifespans Female primates live longer than males Males tend to have riskier lives Dispersal Higher intra-sexual competition More physical fighting E.g., chimpanzees 41% of females survive to 15 years of age 27 % of males survive to 15 years of age 9 8  03/20/2025 Non-human primate babies: Single, generally unassisted births - Exceptions: Callitrichids Grasping hands When infants aren’t parked, they are carried 24-7 - Continuous opportunity to learn through observation & experience 10 9  03/20/2025 Altricial Precocial Undeveloped Well developed Primate infant brains are fairly under- Active or physically mobile at birth developed at birth http://www.dailykos.com http://ecobirder.blogspot.ca http://ecodevoevo.blogspot.ca 11 10  03/20/2025 Primate infants are costly More altricial Less altricial Strepsirhines Haplorhines Lemurs and lorises Tarsiers, monkeys, and apes 12 11  03/20/2025 Comparing primate infants Mothers are parkers Mothers are carriers Some lemurs and lorises Most haplorhines Short lactation Long lactation Post-partum mating No post-partum mating *In callitrichids and pair living cebids (owl monkeys), males and older siblings are communal carriers 13 12  03/20/2025 Natal (infant) coat Infants are a different colour than adults Signals need for care Encourages allomaternal investment. Identifies infants easily Helps group members recognize and protect them. Reduces aggression Adults are less likely to harm or reject distinctively colored infants. 14 13  03/20/2025 New infants often draw attention from other group members www.nature.com 15 14  03/20/2025 Socialization: Modification of behavior through observation of and interaction with others in the social group. Begins very early on in life and can occur when infants play and explore or just through general interactions http://pixabay.com 16 15  03/20/2025 Socialization is important in primates Large brain relative to body size Slow maturation Lengthy period of dependence Heavy reliance upon learning for survival F. Campos E. Visalberghi 17 16  03/20/2025 Infant socializing agents: Mothers Adult males Allomothers Peers 18 17  03/20/2025 The mother- offspring bond is very strong It may persist throughout life 19 18  03/20/2025 Maternal Care Mothers nurse their own offspring Recognition visual, olfactory and auditory clues Rare mix-ups Kidnapping Death Adoptions 20 19  03/20/2025 Variability in Maternal Care 1. Age of the mother 2. Parity of the mother (experience) Nulliparous, primiparous, multiparous 3. Rank of the mother 4. Temperament of the mother 5. Temperament of the infant 6. Species differences 7. Sex of the infant 21 20  03/20/2025 Variability in Maternal Care 22 21  03/20/2025 Infant socializing agents: Mothers Adult males Allomothers Peers 23 22  03/20/2025 Adult male – infant interactions Not well studied Why do males interact with infants? Sexual Selection and female choice Parental investment Paternity certainty Kin Selection siblings, other maternal kin 24 23  03/20/2025 Paternal Care Indirect: Tolerance, detection and defense against predators, resource defense for the group Direct: Direct male care is favored when infants require a high level of investment (e.g., callitrichids) Male care is predicted to be higher when paternity certainty is higher (monogamy) 25 24  03/20/2025 5 categories of adult male – infant interactions/relationships Use and Occasiona Intensive Tolerance Affiliation abuse l affiliation caretaking 26 25  03/20/2025 Intensive caretaking Males spend large portion of day in infant caretaking Parental duties =shared (carrying, protecting, sharing food) Male care ends when infant capable of independent movement A tamarin male carrying his twins Most common in monogamous NWM P. Oxford 27 26  03/20/2025 Callitrichids Infants spend 50 to 90% of their time away from their mothers being carried by their fathers Nonmaternal caregivers also provide solid food http://www.thisisdevon.co.uk Help is critical to infant’s Male silvery marmoset + twins survival 28 27  03/20/2025 Prolactin Females: prolactin stimulates the mammary glands of mothers to make and secrete milk Elevated levels of prolactin also found in males who participate in parental care e.g. cotton-topped tamarins 29 28  03/20/2025 Paternal Prolactin Males carrying infants had high levels of prolactin prolactin levels of infant carrying Ms are similar to nursing Fs Differences between experience vs. inexperienced fathers http://alisaterry.blogspot.ca Prolactin inhibits Male Cotton-topped tamarin testosterone 30 29  03/20/2025 What comes first? Does prolactin stimulate caregiving? Or does caregiving stimulate the production of prolactin? Prolactin comes first. Paternal prolactin levels are a response to hormonal or behavioral cues from the pregnant females 31 30  03/20/2025 Affiliation All/most males spend part of day in friendly interactions with one or more specific infants Not intensive caretaking, but does involve enduring relationships (Males are often “friends” with the mother) Infants attracted to males and form bonds, turn to them in times of distress Males “babysit” while mother is away Males protect infant from other group members http://travel.mongabay.com 32 31  03/20/2025 Occasional affiliation and Tolerance Males typically tolerate infants (permit infants to be near them) but rarely direct affiliative behaviors toward them Males may show occasional affiliative behaviors, such as brief social interactions or play, but do not consistently invest in infant care. Interactions often opportunistic rather than a regular pattern of paternal care. E.g., Japanese & rhesus macaques http://www.treknature.com 33 32  03/20/2025 Use and abuse Males interact in ways which are beneficial to the male, potentially harmful to the infant Agonistic buffering (triadic male-infant interactions) Males grab or hold an infant during conflicts with other males. May reduce the likelihood of aggression from opponents, as attacking a male holding an infant could harm the infant and provoke the mother. Strategy advantageous to the male but dangerous for the infant. Mothers may resist Mothers may be drawn in to support the I. Yufera male 34 33  03/20/2025 5 categories of adult male – infant interactions/relationships Use and Occasiona Intensive Tolerance Affiliation abuse l affiliation caretaking 35 34  03/20/2025 Extreme end of continuum: Infanticide More about that when we discuss sources of infant mortality 36 35  03/20/2025 Infant socializing agents: Mothers Adult males Allomothers Peers 37 36  03/20/2025 Allomothering Allo = other Who (besides mother & potential sire) cares for or interacts with infants? Female kin Juvenile females 38 37  03/20/2025 Why show interest in taking care of someone else's infant? 1. Learning to mother hypothesis Who benefits? The alloparent Individual selection 2. Mother relief hypothesis Who benefits? The mother Kin selection & inclusive fitness Both benefit if the allomother is kin The allomother gains experience, and the mother gets relief, while the behavior increases the survival chances of shared genes (inclusive fitness) 39 38  03/20/2025 Alloparenting or Infant handling Very young infants http://www.cbc.ca handled most Subadult/nulliparous females handle most Cases of affiliative infant handling and neglect/abuse http://www.naturalhistorymag.com 40 39  03/20/2025 Alloparenting in Cercophitecides Colobines Cercopithecines Egalitarian Despotic/ Hierarchical High levels of Lower levels of allomothering—females allomothering—mothers readily share infant care. are more protective. Infants frequently handled, Infant handling is rank- even by non-mothers. dependent (HR females have more access). More permissive in allowing others to carry, Mothers may limit groom, and interact with interactions due to risk of infants. kidnapping or harm. 41 40  03/20/2025 Infant socializing agents: Mothers Adult males Allomothers Peers 42 41  03/20/2025 Peers & play Young primates interact with age mates First experience interact with non-relatives First opportunity to learn social skills outside of kinship context Photo: http://www.dailymail.co.uk 43 42  03/20/2025 Play Play is easy to recognize, but hard to define Characteristics of play: Exaggerated Repeated Restrained Often accompanied by a “play face” E.g., running as play is exaggerated, loose, relaxed E.g., fighting as play is restrained 44 43  03/20/2025 Play can be: Solitary Solitary with objects in the environment Social with others Function of play? Practice for adult skills – physical & social Teaching Bonding Skill acquisition/demonstration Juvenile chimpanzees playing, Pan Stress relief troglodytes Learning (photo credit: K. Amman) 45 44  03/20/2025 Play & Social organization Who they have to play with depends on group composition & dispersal MM-MF female-bonded – play with kin & friends Monogamous – play with neighbours, sibs, parents - solitary play common 46 45  03/20/2025 INFANT MORTALITY Disease Stochastic events Infanticide 47 46  03/20/2025 Infant mortality: Disease Ectoparasites, gastrointestinal parasite infections, Ebola, yellow fever, various unknown infectious diseases... http://www.cbc.ca Chacma baboons: 50% of all infant mortality was attributed to tick infestations in one population 48 47  03/20/2025 Infant mortality: Stochastic events Difficult to determine % of infant deaths attributed to predation Crowned Hawk Eagle + infant monkey 49 48  03/20/2025 Infant mortality: Infanticide The link with lactation time: Lactation Time / Gestation Time Females with long lactation periods tend to undergo postpartum amenorrhea + no post-partum mating occurs Loss of infant = female resumes estrus sooner 50 49  03/20/2025 Comparing primate infants Mothers are parkers Mothers are carriers Some lemurs and lorises Most haplorhines Short lactation Long lactation Post-partum mating No post-partum mating *No infanticide (and no infanticide in *Infanticide occurs communal carriers) 51 50  03/20/2025 Correlates of infant care & infanticide Parkers Carriers Lactation>gestation 0 95% Post-partum mating 82% 0 Male infanticide 0 49% % are generated from pooled species Adapted from van Schaik (2000) 52 51  03/20/2025 Parent-Offspring Conflict: Weaning Weaning is a major time for conflict Offspring demand more from their mothers (& fathers) than they are willing to give Mother stops investing in the offspring sooner than it wants Hanuman Langur 53 52  03/20/2025 Sex differences in weaning Mothers might be expected to wean one sex later than others if the extra investment translates into higher maternal inclusive fitness E.g., High-ranking chimpanzees: Females invest more in sons than daughters, weaning sons later 54 53  03/20/2025 Juvenile Period from weaning to sexual maturity Unlike infants, likely to survive death of mother 55 54  03/20/2025 2 strategies to surviving being a juvenile Strategy Example Minimize time spent 1 as a juvenile Strepsirhines 2 Grow slowly Haplorhines 56 55  03/20/2025 Growing Slowly Benefit: Niche separation Small-body allows feeding on terminal branches 57 56  03/20/2025 Growing slowly Cost: Increased vulnerability to predators Chacma baboons being chased by lions 58 57  03/20/2025 Growing slowly Cost: Feeding efficiency and diet < adults Female yellow baboons who had a poor juvenile diet: Shorter reproductive lifespans Produced fewer offspring, of which fewer survived 59 58  03/20/2025 Juvenile social skills Relationships are established through play 60 59  03/20/2025 Puberty Hypothalamus > secretes hormones > activates pituitary gland > affects the gonads Testis Ovaries Stimulated to produce Stimulated to produce progesterone and testosterone estrogen 61 60  03/20/2025 Secondary sex characteristics appear 62 61  03/20/2025 Puberty: Transition to adulthood More gradual for males than females Dispersal usually takes place before puberty or before dispersing individual becomes sexually active High mortality increased predation risk, aggression from other groups, challenge on finding food/allies Reproduction demands 63 62  03/20/2025 Sex differences in behavior Become most obvious at puberty Do exist in infants in some species E.g., rhesus macaque male infants show: More assertive/aggressive behavior More rough & tumble play More independence from their mothers Less interested in grooming Less interested in infants 64 63  03/20/2025 Adulthood More or less continuous from puberty to death No major stages or categories within the adult life course 65 64  03/20/2025 Sex differences in social relationships based on dispersal Patrilocal Matrilocal J. Mitani 66 65  03/20/2025 Ageing No distinct social role or behavior for old NHP’s as there is for humans Why? Division of Labour Awareness of Mortality Menopause 67 66  03/20/2025 Division of Labour Non-human primates Humans Do not share food Share food Each individual is a complete Depend on a system of production subsistence unit and exchange No opportunity to become Individuals are highly dependent on others interdependent Change in ability to produce will Loss of ability to feed oneself = change social role, but does not death usually result in death 68 67  03/20/2025 Awareness of Mortality Non-human primates Humans Unlikely to be aware of own Aware of our mortality mortality Unlikely to be objects unto Able to think about ourselves as themselves separate and temporary Unlikely to be aware that they are Know that we will die, and that old temporary, society will go on age leads to death Give meaning to biological No anticipation that death is changes, anticipate mortality, coming with old age change behavior 69 68  03/20/2025 Menopause in NHP?  Menopause: reproductive cessation but other organ systems remain healthy-- may be unique to human females  Chimps: only 7% of wild chimps reach age 40; but tend to remain fertile until death http://www.janegoodall.ca 70 69  03/20/2025 Menopause Non-human primates Humans Occasional reproductive A universal (population-wide) termination midlife occurrence Not temporally distinct from the Temporally distinct from the overall overall advanced aging of the ageing of the organism organism Occurs very late in life Occurs in healthy middle age Is not associated with increased Associated with increased production or survivorship of survivorship of grandchildren grandchildren 71 70  03/20/2025 Grandmother hypothesis Hadza hunter & gatherers in Tanzania (Hawkes et al 1997) Grandmothers who help raise/ provision their grandchildren increase their daughter’s fertility -Shorten inter-birth interval -Provisioning helps grandchildren gain weight 72 71  03/20/2025 Grandmother Hypothesis: Menopause is directly adaptive via increases in the production or survivorship of descendants. Women stop reproducing because there are greater fitness benefits to be had by helping your daughters and grandkids than by having more babies yourself. 73 72  03/20/2025 Ageing Experience of old animals depends on the social organization of the group/species, and the reproductive history of the individual Rest more & feed less Kin-based Older females in matrilocal societies tend to stay integrated Older males in patrilocal species can become more socially isolated, especially if they fail to maintain dominance 74 73  03/20/2025 Videos Rhesus macaques Puerto Rico 75 74  03/20/2025 Summary Primates have slow life histories Infants tend to be altricial and dependent on social learning Mothers are the main caretakers Other individuals are also important Peers become more important during juvenilehood Puberty leads to higher mortality for the dispersing sex Adulthood is a long, continuous state Ageing is less pronounced in NHP’s compared to humans Menopause may only occur with regularity in humans The grandmother hypothesis may explain the existence of menopause in humans 76 75