Primate Social Systems - Diversity

Extant Primate Taxonomy

• Strepsirrhini

  • Lemuriformes

    • Lemuridae: ring-tailed lemurs, true lemurs, ruffed lemurs, bamboo lemurs

    • Indriidae: indris, sifakas, woolly lemurs

    • Lepilemuridae: sportive lemurs

    • Cheirogaleidae: mouse lemurs, dwarf lemurs, fork-crowned lemurs

    • Daubentoniidae: aye-ayes

  • Lorisiformes

    • Lorisidae: lorises, pottos

    • Galagidae: galagos

• Haplorhini

  • Tarsiiformes: tarsiers

  • Anthropoidea

    • Platyrrhini

      • Cebidae

        • Pitheciidae: titis, sakis, uakaris

        • Atelidae: spider monkeys, muriquis, woolly monkeys, howlers

        • Callitrichinae: marmosets, tamarins

        • Aotinae: owl monkeys

        • Cebinae: capuchins, squirrel monkeys

    • Catarrhini

      • Cercopithecoidea: Old World monkeys

      • Hominoidea: apes, humans

Archonta

• Order Primates

  • Semiorder Euprimates (primates of modern aspect)

    • e.g., Omomyidae, Adapidae

  • Semiorder Plesiadapiformes (archaic primates)

    • e.g., Carpolestidae (Carpolestes), Paromomyidae, Micromomyidae, Plesiadapis

• Order Scandentia (tree shrews)

  • e.g., Ptilocercus

• Order Dermoptera (flying lemurs)

• Order Chiroptera (bats)

Primate Social Systems

• Definition: Social organisation + social structure + mating system.

• Key Question: How many different types of social systems do primates have?

How are primate groups different?

• Individual recognition: The basis for complex social interactions.

  • Birds and mammals recognize individuals.

  • Many species without parental care or bonding probably lack this.

  • Other species only recognize categories (e.g., colony member or not).

  • Anonymous societies.

• Stability of association: Membership changes through births, deaths, immigration, and emigration.

• Individual recognition + stable association --> individualised societies (= fundamental social units).

Components of a Social System (Society)

• Social organisation (group size, composition and stability)

• Social structure (patterning of social relationships)

• Mating system (has both a social and genetic element)

• Spatial association

• Social interactions

1. Social Organisation

• Size, sex composition, and spatio-temporal cohesion of social units.

• Spatial overlap has to coincide with social boundaries --> Social unit.

• Variability in a population or species:

  • The extent of variation in spatio-temporal dynamics.

  • The degree to which the modal social organisation is realised within a population.

    • Uniformly: > 90% of social units.

    • Variably: <90% of social units.

• 5 main types of social organisation:

  1. Solitary

  2. Pair

  3. One-male-multi-female group

  4. Multi-male-multi-female group

  5. Multi-male-one-female group

Spatio-Temporal Dynamics (in group-living primates)

• Troops:

  • Predictable membership; all together all day.

  • E.g., gorillas, baboons, vervets

• Fission-fusion societies:

  • Predictable (stable) community membership

  • Unpredictable party membership

    • (a) ’Atomistic’ parties - down to 1; E.g., chimpanzees, spider monkeys

    • (b) ’Molecular’ parties - down to predictable subgroups; E.g., hamadryas baboons, geladas

2. Social Structure

• Emergent property of dyadic relationships.

• Relationship = repeated social interactions between individuals.

• Types of social interactions:

  1. Affinitive - indicate a spatial association

  2. Affiliative - friendly

  3. Agonistic - aggression and submission

• Dispersal patterns - strong influence on social structure: They determine the availability of social partners!

3. Mating Systems

• Some overlap with social organisation (but not always).

• Social mating system (mating behaviour) vs. genetic mating system (the reproductive outcomes).

  1. Monogamy

  2. Polyandry

  3. Polygyny

  4. Polygynandry

• Mating also occurs outside the social unit (extra- pair or extra-group paternity).

A. Solitary Primates

• Mostly nocturnal (except orangutan).

• Difficult to study (the nocturnal ones)!

• Forage alone.

• Little coordination between individuals in space and time.

• But they still have social relationships and social networks ( ~ social structure).

• Solitary $\neq$$$\neq$$ asocial!

  • Mothers + offspring

  • Sleeping groups

  • Communication (auditory and olfactory)

• Goodman’s mouse lemur (Microcebus lehilahytsara)

• Up to 1/3 of all primate spp. [or only 6%!?!]

• Most lorisiforms (except Galagoides zanzibaricus)

• Several species of:

  • Tarsius

  • Daubentonia

  • Microcebus

  • Allocebus

  • Mirza

• Some Cheirogaleus and Lepilemur

• Pongo spp. (~ semi-solitary)

• Hairy-eared dwarf lemur (Allocebus trichotis)

B. Pair-Living Primates

• The rarest type of social organisation in primates (and mammals).

• But more common in primates than in mammals! (~15% or 23% VS ~3-4%).

• Two types of pairs:

  1. Dispersed: M and F not together all the time

  2. Gregarious: permanent association between M and F

• Male care for offspring is common (but not always obligate).

  • Titi monkeys - obligate

  • Gibbons - no direct care (e.g. infant carrying)

• Pair-living is not = reproductive monogamy! Extra-pair copulations happen.

• The adaptive basis of pair-living still debated…

2. Pair-living primates: dispersed pairs

• Strepsirhines e.g.: Galagoides zanzibaricus, Cheirogaleus medius, Phaner furcifer, Lepilemur edwardsi, Lepilemur ruficaudatus

• M and F range overlap closely.

• Defend together.

• But M & F not consistently associated, or sleeping together….

• Fork-marked lemur (Phaner furcifer)

2. Pair-living primates: gregarious pairs

• Pairs with offspring (up to several generations)

• Extensive paternal care (probably obligate!)

• Up to 90% of time infant is carried by father

• Playing, grooming and food sharing with infant

• Siblings don’t help.

• Living in pairs: Rare, explanation needed (or is it??)

• Costs/benefits from the perspective of each partner?

• Particularly interesting --> understanding the evolution of human pair bonds.

(C) Group-Living Primates

• One-male, many females (Unimale groups; One- male units = OMUs) ~ polygynous mating system

• Multi-male-one-female groups ~ polyandrous mating system

• Multi-male-multi-female groups ~ polygynandrous mating system (but some exceptions, e.g. in the multi-level societies of geladas, hamadryas baboons, etc. with 1-male units as the lowest level or organisation)

One-Male Units

• Both sexes can disperse

• Typically, a strong bond between females and the male

• Weaker bonds among females (but sometimes can be relatives)

• Bachelor groups common

• Highly polygynous

• Intense male-male competition for breeding opportunities

Geoffroy’s tamarin, Saguinus geoffroyi

• Tamarins: Need help to rear twins (combined weight 20% of mother’s weight at birth and 50% at weaning).

• Infants carried at all times.

• Mothers need to feed much more when raising offspring (high cost of lactation!)

• Groups with more males taking care of offspring have more surviving offspring. --> Facultative polyandry

• Co-breeding males are usually related (likely brothers)

(C) Group-living primates

• Troop-living (spatially and temporally cohesive groups), e.g. rhesus macaques

• Fission-fusion societies (fluid membership) with temporary parties (subgroups)

  • Atomistic parties, e.g. chimpanzees

  • Molecular parties -> multi-level societies (e.g. hamadryas baboon)

Rhesus Macaques

• Stable groups

• Female philopatric --> matrilines within groups

• Males move to new groups when sexually mature; queue for dominance

Chimpanzees

• Fission-fusion society

• Male philopatric --> coalitions with kin

• Females leave natal group when sexually mature

• Adult females (particularly mothers) are much less gregarious than males

• Male chimpanzees more gregarious than females

Multi-Male, Multi-Female Societies

• Multilevel societies (down to ‘molecular’ stable parties)

  • Geladas

  • Hamadryas baboons

  • Snub-nosed monkeys

  • Capped langurs

  • Proboscis monkeys

Multi-Level Organization in Hamadryas Baboons

• Individuals

• Family

• Clan : 10-20

• Band : 30-100

• Troop : > 600

Multi-Level Societies

• Multi-level societies: the most complex societies.

• Primates:

  • Papionins (gelada, Hamadryas baboon, Guinea baboon).

  • Asian colobines (snub-nosed monkeys, proboscis monkey, douc langurs).

  • Maybe also in: uakaris, drills, Angolan colobus…

• Other mammals: elephants, zebras, giraffes, sperm whales

• Often in species where food competition is not too high (e.g. grass foraging) - e.g. gelada, zebra…

• Often pronounced sexual size dimorphism.

• Exaggerated secondary sexual traits (e.g. chest patches, big nose… ) to act as ‘badges’ in a large society where not everyone knows all other members!

• Cognitive consequences largely unexplored but could be significant.

What was the social organisation of the ancestral primates?

• Nocturnal, small, arboreal, solitary?

Phylogenetic analysis of sociality

• Phylogenetic inertia in behavioural traits --> allows the use of Bayesian statistics to infer changes through time.

• N = 217 species examined.

• Classified as: Solitary (purple), Family groups (pink), Harems/one-male groups (orange), Multi-male (red)

• Analysis showed a strong phylogenetic signal in the data (Pagel’s lambda = 0.983)!

Models for the evolution of sociality

• Three alternative models for the evolution of sociality:

  • Increasing complexity

  • Equal rates (null) and parameter rich

  • Reversible-jump model

• Best support: reversible-jump model

• Estimated transition rates for co-evolution of social living: Switch to social living - alongside switch from nocturnal to diurnal living

• The model with the highest posterior support for the evolution of stable or bonded social groups implies that stable social groups evolve from sociality through unstable social groups.

• Strong support for the importance of predation: group living co- evolved with the transition from nocturnal to diurnal life.

• Sociality based on loose aggregations followed by second shift to stable or bonded groups --> importance for the evolution of cooperation within groups! (implication for the evolution of coalition formation, resource defense and large brains).

Olivier et al. 2024 PNAS

• 493 populations from 215 species

• Only field data

• Explicitly considered intra-specific and intra -population variation in social org

• High rates of pair-living: primary for 16% of populations and 23% of species

• Low rates of solitary: primary for 3% of populations and 6% of species

• 64% of species and 43% of populations had more than one type of social organisation

• IVSO = intrapopulation variation in social organisation

• Ancestral state reconstruction: Under the assumptions of small body size (~50 g) + arboreality + nocturnality (based on fossil evidence)

• Statistical models identified pair-living (MF) to be the most likely primate ancestral state

• ~15% of social unit in ancestral populations would be solitary

• Variable social organization with most individuals being pair-living

• Differences in classifying social systems can influence interpretation of data.

• Solitary living is a derived state – and an adaptation to specific environmental conditions.

PRIMATE SOCIAL SYSTEMS

• Complex individualised societies.

• Three descriptive axes of variation (social organisation, social structure, mating system).

• Diversity found across all taxa and sometimes within taxa (although some types of social system are restricted in distribution - e.g. solitary are mostly nocturnal).

• Special interest ~human evolution: pair-living/social monogamy; multi-level fission-fusion societies.Primate social systems