Evolution of social behavior

1. Evolution of social behavior Topics for this class: • What is behavioral ecology? • Group selection vs. individual selection controversy • Altruistic social behavior via individual selection mechanisms • Kin selection--genetics • Kin selection--ecology • Reciprocal altruism • Non-altruistic group living (flocks, herds, aggregations)

2. What is behavioral ecology? • Define behavioral ecology as the study of animal behavior using genetic and ecological hypotheses • Sister field of evolutionary ecology….big q. was, at what level of organization does evolution occur? Individual-population-species? • Useful to ecologists by explaining patterns of distribution and abundance: e.g., group size, habitat preferences, dispersion (distribution) patterns, regulation of abundance, etc…...Environmental factors also apply….. • Deals with both ultimate explanations (why does a behavior occur, why did it evolve?) and proximate explanations (what is the immediate cause of the behavior, such as drive or physiological mechanism). • …..Lots of work done w. idea of animal behavior to understand human behavior

3. Group vs. individual level selection: alternative mechanisms for behavior • Alternative 1- Social behavior as mechanism of population self-regulation • Benefit of self-regulation would be avoidance of ravages of starvation, disease, risky contests with other animals • This would necessitate group-level natural selection, I.e., groups of individuals are favored with increased survival within a population (thus produce more offspring overall) that cooperate by showing reproductive restraint • Example: Alexander Skutch explained tropical birds’ small clutch size (few eggs) as self-restraint to avoid wastage of scarce tropical resources

4. Group vs. individual level selection: alternative mechanisms for behavior • Alternative 2: Social behavior as result of individual-level selection • Individuals act in their own selfish interests, reproductively, to produce as many offspring as allowed by ecological constraints • E.g., David Lack explained small clutch size of tropical birds by constraint of less food in tropics and reduced feeding time at low latitudes (12 hours daylight in summer in tropics, vs. >12 h at higher latitudes) • Reginald Moreau-yes but….

5. what about Social Behaviors? • V.C. Wynne-Edwards (1962): “Animal dispersion in relation to social behavior” • Hypothesized most social behaviors are mechanisms of reproductive self-restraint (much as Skutch argued for clutch size in birds) • E.g., group displays (flocking, evening roosts, aggressive contests between males) as “epideictic displays” = population size-assessment mechanism…(ie the mechanism allowing altruistic cooperation.)

6. Response to Wynne-Edwards: strong criticism • Most important criticisms, mid 1960’s, by G.C. Williams, David Lack • Mutation argument--selfish gene mutation would prevail over altruist gene (latter not an “evolutionarily stable strategy”) • Immigration argument--selfish invader would prevail • Individual selection argument--all Wynne-Edward’s behaviors could be explained by individual level natural selection • Resource prediction--little evidence to indicate that individuals can predict future resource levels, a condition for group-selection interpretation of social behaviors • What are the prevailing, individual-level explanations for social behaviors? This is topic of rest of lecture.

7. Evolution of social behavior via kin selection • Altruism is one kind of social behavior that is particularly challenging to explain (e.g., grooming of other individuals, alarm calls, sacrificing reproduction or one’s life for another individual) • Such sacrifice reduces one’s energy, and one’s direct reproduction, so how could it evolve via natural selection acting to maximize individual fitness? • Darwin acknowledged (in “On the origin of species…”) that bee & wasp behavior of sacrificing individual’s life to defend colony countered his mechanism of natural selection

8. Theory of kin selection via genetics • W.D. Hamilton provided explanation this century, based on genetics • His idea is termed inclusive fitness, with two parts: • Direct fitness involves genes passed to future generations directly via one’s offspring (the only form of fitness Darwin knew) • Indirect fitness involves genes passed to future generations indirectly, via relatives sharing one’s genes • Hamilton’s rule: Gene will spread via kin selection if rB - C > 0; r = coefficient of relatedness, B = benefit (offspring gained by recipient), C = offspring cost that altruist sacrifices genetically; same equation: B/C > 1/r

9. Example of kin selection: eusociality in social Hymenoptera • In diploid organisms, like humans, genetic relatedness, r, is at most 0.5 (to father, mother, siblings, offspring), and less to more distant relatives (0.25 to grandson, granddaughter; 0.125 to cousin) • Thus Hamilton’s rule: B/C > 1/(1/2), i.e., B/C > 2 • In words, ratio of benefit to recipient of altruistic act must be twice as large as cost to donor (a difficult condition to meet) • For the altruist to benefit ALSO, the ratio of benefit for the recipient must be 2X the cost to the altruist (donor).

10. What’s so unusual about social Hymenoptera (ants, bees, wasps)? • Social Hymenoptera inherited a different genetic system, haplodiploid, in which males are haploid (unfertilized eggs) and females are diploid (fertilized) • Values of r are different as result: sisters have relationship of 0.75; sister-brother r = 0.25; mother-daughter r = 0.5 • Hamilton’s rule for sisters? B/C > 1/(3/4) ==> B/C>4/3 • Thus for sisters, barrier to altruistic behavior lower • Indeed, social Hymenoptera evolved highly social (“eusocial”), altruistic behavior multiple times, in all cases involving cooperation (altruism) among sisters

11. What is eusociality? • Define eusociality as the highest level of organization (greatest degree) of socially living organisms, defined by three conditions: • Reproductive division of labor (castes) • Cooperative care of offspring • Overlapping generations within a nest • Many social Hymenoptera meet all these conditions (involving females) • Humans are social (& even sometimes anti-social!), but certainly not eusocial (human societies don’t manifest all three conditions above)

12. Theory of kin selection via ecological disposition: • Problem with Hamilton’s idea is that it can’t explain eusociality in termites (diploid, genetically) or naked mole rats (also diploid; and the only mammal that exhibits eusociality)….what’s up in these animals? • R. Alexander proposed ecological conditions as alternative explanation for altruism & eusociality: • Confinement to burrows or nests (Cities?) • Food abundant enough locally to support dense population • Adults exhibit parental care • Mothers can manipulate other individuals (-->castes)

13. Sociality via reciprocal altruism • Theory: individuals--that are not necessarily related genetically--reciprocate over time in assisting each other (“you scratch my back, and I’ll scratch yours”) • Three conditions generally considered necessary for function of reciprocal altruism: • Individuals must recognize each other (to keep tabs on level of cooperation from other interacting individuals) • Interactions among individuals are long-term, e.g., in primate troop (or human village) • Retaliation in cases that individuals violate “pact” (i.e., individuals play “tit-for-tat” kind of game, cooperating when other individual cooperates, and retaliate when other individual does not cooperate)

14. Examples of social behavior via reciprocal altruism • Grooming and coalitions in female vervet monkeys • Reciprocal altruism likely the lynch pin of human social behavior! (explains human emotions, & ethics--e.g., work of Franz DeWaal)

15. Some mechanisms of non-altruistic group-living • Disadvantages of group living: • Competition for food, nests, mates • Increased risk of predation, parasitism • Compensating advantages of group living • Predator-avoidance--many eyes, distraction effect, group defense, selfish herd • Feeding efficiency--e.g., learning good food source from flock member; cooperative hunting as in wolves • Mating opportunities--extra-pair copulations within reproductive colonies (e.g. least flycatcher)

17. Tradeoffs can moderate flock size

18. Aggregated (clumped) distribution of least flycatcher territories, Hubbard Brook, NH (dots, far left are 50 m apart; bird territories are circles in right panel). (From Sherry & Holmes, 1985)

19. Why do least flycatchers aggregate into clusters of breeding territories? • Tom Sherry studied this with Peter Yaukey years ago (he’s now professor at UNO) • No compelling evidence for predator-defense (they used caged blue jay to simulate nest predator) • No obvious feeding advantage to birds in larger colonies • Scott Taroff (Queen’s University, Canada) now argues that the advantage is mating opportunities: • Least flycatchers mate outside pair-bond (extra-pair copulations--based on DNA fingerprinting) • Older males and females both benefit from larger number of neighbors (younger males lose out--by being cuckolded by older males)

20. Conclusions: • Social behavior (large group size, dense local population) can result from a variety of factors--genetic, ecological • Groups can result because of feeding opportunities, defense against predators, mating opportunities that individuals can use to their own advantage • A wide variety of social behaviors can be explained simply on the basis of individual-level natural selection, and individual (selfish) reproductive advantages--even altruistic behaviors such as seen in eusocial animals • Behavioral ecology has provided a rich source of new data, and ideas to explain animal distributions and other behaviors