Behavioral Ecology P5

Fundamentals of Social Interactions and Cooperation

Categorization of Social Interactions:
- Behavioral ecologists classify social decisions based on their fitness effects on two key actors:
  - Actor: The individual performing the behavioral act.
  - Recipient: The individual affected by the actor's behavioral act.
- The Four Classes of Social Interactions:
  - Mutual Benefit: The behavior increases the fitness of both the actor ( $+\text{actor}$ ) and the recipient ( $+\text{recipient}$ ).
  - Selfishness: The behavior increases the fitness of the actor ( $+\text{actor}$ ) while decreasing the fitness of the recipient ( $-\text{recipient}$ ).
  - Altruism: The behavior decreases the fitness of the actor ( $-\text{actor}$ ) while increasing the fitness of the recipient ( $+\text{recipient}$ ).
  - Spite: The behavior decreases the fitness of both the actor ( $-\text{actor}$ ) and the recipient ( $-\text{recipient}$ ).

Historical Perspectives on Altruism:
- Charles Darwin: Recognized that natural selection readily favors mutually beneficial behaviors, but viewed altruistic acts as a major challenge to evolutionary theory because natural selection should eliminate behaviors that reduce individual fitness.
- Group Selection Hypothesis: Proposed that altruistic individuals sacrifice their personal fitness for the collective good of the species or group (e.g., individuals voluntarily forgoing reproduction so the population does not exhaust its food supply).
- Debunking Group Selection: George Williams successfully debunked the group-selectionist argument by demonstrating that individual selection is significantly stronger than group selection, meaning group selection cannot explain the origin or maintenance of altruism.

Vampire Bats and the Evolution of Reciprocity

Ecology of the Common Vampire Bat (Desmodus rotundus):
- Roost in communal colonies in places such as caves in Costa Rica and Mexico.
- Emerge nightly to feed stealthily on mammalian blood (e.g., horses, mules).
- If a bat is detected by its host prey, it gets shaken off prior to feeding.
- On any given night, up to $30\text{\%}$ of colony members fail to obtain a blood meal.
- Starvation threshold: A bat that fails to feed for several consecutive nights will starve to death.

Altruistic Meal Sharing:
- Starvation is mitigated because successful bats regurgitate blood meals to hungry colony members begging for food.
- Blood sharing is observed exclusively among female roostmates.
- Cost-Benefit Asymmetry:
  - The relationship between body mass (% pre-fed weight) and hours until starvation is non-linear.
  - A donor bat giving up a unit of blood loses relatively few hours until starvation, whereas a recipient receiving that same amount gains a significantly larger number of hours until starvation.
  - Therefore, donors give up less time until starvation than recipients gain.

Graph plotting body mass change over time since feeding

Conditions for Reciprocity (Robert Trivers):
- Robert Trivers proposed that seemingly altruistic acts are examples of reciprocal altruism ("if you scratch my back, I'll scratch yours").
- Reciprocity can evolve if three strict conditions are met:
  1. The benefit to the recipient exceeds the cost to the actor ( $B > C$ ).
  2. There are frequent opportunities for mutual repayment over time.
  3. Individuals can recognize one another and track past behaviors.
Empirical Evidence in Vampire Bats (Carter and Wilkinson, 2013):
- Female vampire bats form stable social associations lasting over multiple years, providing frequent opportunities to repay shared blood meals.
- A multivariate statistical model ( $\text{overall } R^2 = 0.38$ ) evaluated factors predicting blood donation:
  - Food received previously: By far the strongest predictor (relative importance of $0.5$ ; $8.5\times$ more important than genetic relatedness).
  - Sex of donor: Second highest predictor.
  - Social grooming received previously: Third highest predictor.
  - Relatedness: Lowest relative importance among significant variables.
- These empirical findings strongly confirm that blood sharing in vampire bats is primarily maintained by reciprocity rather than simple kin preference.

Game Theory and the Vampire Bat's Dilemma

Single-Round Play (The One-Shot Vampire Bat's Dilemma):
- Modeled as a variation of the classical Prisoner's Dilemma.
- Two basic strategies:
  - Share: Donate blood to a hungry roostmate.
  - Withhold: Keep all blood for oneself.
- Payoff Matrix (Fitness gained in hours until starvation):
  - Both Share: Both receive a payoff of $6$ .
  - Player 1 Shares, Player 2 Withholds: Player 1 gets $-3$ ; Player 2 gets $9$ .
  - Player 1 Withholds, Player 2 Shares: Player 1 gets $9$ ; Player 2 gets $-3$ .
  - Both Withhold: Both receive a payoff of $0$ .
- Optimal Payoff Choices:
  - If the opponent Shares: Withholding yields $9$ , which is greater than Sharing ( $6$ ).
  - If the opponent Withholds: Withholding yields $0$ , which is greater than Sharing ( $-3$ ).
- Evolutionarily Stable Strategy (ESS) in Single-Round Play:
  - Withhold is a pure ESS. In a population playing a single round without memory, defection always invades and displaces cooperation.
Repeated Encounters (Iterated Vampire Bat's Dilemma):
- Real vampire bats interact repeatedly over years within small, stable colonies.
- In an iterated setting (e.g., 10 rounds with memory), fitness depends on long-term behavioral strategies.
- Common Game Plans Evaluated:
  - Random: Randomly choose to Share or Withhold regardless of opponent actions.
  - Punish: Share until the opponent Withholds, then Withhold permanently for all remaining rounds.
  - Copy (Tit-for-Tat): Mimic the exact strategy played by the opponent in the previous round.
- Outcome: The Copy (Tit-for-Tat) strategy yields the highest individual fitness.
The Tit-for-Tat Strategy (Axelrod and Hamilton):
- Discovered during computer tournaments hosted by Robert Axelrod and William Hamilton.
- Key Rules: Begins by cooperating on turn 1, then mimics the opponent's previous move on every subsequent turn.
- Three Essential Attributes for Success:
  1. Nice: Never defects first; starts with cooperation.
  2. Retaliatory: Immediately punishes defection by defecting on the next move.
  3. Forgiving: Immediately returns to cooperation as soon as a previously defecting player resumes cooperation.

Conditions Promoting the Evolution of Cooperation:
- Cooperation evolves most effectively when individuals repeatedly interact with the same partners and retain long-term memory of partner behavior.

Alarm Calls in Belding's Ground Squirrels

Natural History of Belding's Ground Squirrels (Urocitellus beldingi):
- Colonial, herbivorous rodents inhabiting mountain meadows in the western United States.
- Excavate burrows for winter hibernation and thermal/predator protection during summer.
- Utilize distinct acoustic vocalizations when predators approach:
  - Aerial Predators (e.g., hawks): Short, high-pitched whistle.
  - Terrestrial Predators (e.g., coyotes, badgers, long-tailed weasels): Long, multiple-note trill.

Belding's Ground Squirrel sounding alarm

Sherman's Three Alternative Hypotheses for Alarm Calling (Paul Sherman):
1. Benefits Caller Hypothesis: Calling directly benefits the caller by reducing its individual predation risk (e.g., causing herd panic that confuses the predator).
2. Reciprocity Hypothesis: Calling directly benefits the caller because warned neighbors reciprocate warning calls in future encounters.
3. Alerts Relatives Hypothesis: Calling indirectly benefits the caller by enhancing the survival of genetic kin sharing common alleles.
Demographic Asymmetry in Urocitellus beldingi:
- Females exhibit natal philopatry (remain in their birth colony for life).
- Males disperse to distant colonies upon reaching adulthood.
- Consequently, females live alongside close female relatives and offspring, whereas adult males live among unrelated individuals.
Hypothesis Predictions Matrix:
- Benefits Caller: Calling decreases predation risk for the caller; males and females are equally likely to call; callers do not discriminate against non-callers.
- Alerts Relatives: No specific prediction on caller risk reduction; females are significantly more likely to call than males; callers do not discriminate against non-callers.
- Reciprocity: No specific prediction on caller risk reduction; males and females are equally likely to call; callers recognize individuals and discriminate against non-callers.
Empirical Testing: Terrestrial Predators (Sherman, 1977):
- Over $3000\text{ hours}$ of field observation in California's Sierra Nevada recorded responses to $102\text{ terrestrial predator attacks}$ .
- Observed Results:
  - Females trilled significantly more frequently than expected by chance ( $p < 0.01$ , G-tests).
  - Females with living relatives were far more likely to trill than females without living relatives.
  - Adult males trilled significantly less frequently than expected ( $p < 0.01$ ).
  - Callers were twice as likely to be killed by terrestrial predators compared to non-callers ( $2\times\text{ mortality risk}$ ).
  - Calling history of nearby squirrels had no influence on whether a squirrel called.

Empirical Testing: Aerial Predators (Sherman, 1985):
- Utilized trained Harris's hawks (Parabuteo unicinctus) to simulate $141\text{ aerial attacks}$ .
- Observed Results:
  - Both males and females were equally likely to whistle ( $p > 0.5$ , G-tests).
  - Both callers and non-callers fled immediately to the nearest burrow refuge.
  - Whistling callers were 10 times more likely to escape predation than non-callers ( $10\times\text{ escape advantage}$ ).
  - Calling history of neighbors did not alter the probability of whistling.

Conclusions for Alarm Calling:
- Trills to Terrestrial Predators: Strongly support the Alerts Relatives Hypothesis (Kin Selection). Calling is altruistic and increases personal mortality risk to protect genetic relatives.
- Whistles to Aerial Predators: Strongly support the Benefits Caller Hypothesis (Direct Benefit). Calling is selfish/mutually beneficial because the vocalization directly aids the caller's personal escape.

Relatedness, Kin Selection, and Hamilton's Rule

Coefficient of Relatedness ( $r$ ):
- Quantifies the probability that two individuals share alleles that are identical by descent from a common ancestor.
- Ranges from $0$ (completely unrelated individuals) to $1$ (monozygotic twins / identical genomes).
Standard Relatedness Values ( $r$ ) in Diploid Species (assuming unrelated parents):
- Parent and Child: $r = 0.5$
- Full Siblings: $r = 0.5$
- Half Siblings: $r = 0.25$
- Aunt/Uncle and Niece/Nephew: $r = 0.25$
- Grandparent and Grandchild: $r = 0.25$
- First Cousins: $r = 0.125$
Inclusive Fitness Framework:
- Direct Fitness: Reproductive output gained through an individual's own direct production of offspring.
- Indirect Fitness: Reproductive output gained by helping genetic relatives reproduce, weighted by their degree of relatedness ( $r$ ).
- $\text{Inclusive Fitness} = \text{Direct Fitness} + \text{Indirect Fitness}$
Hamilton's Rule (William Hamilton):
- Formalizes the condition under which an altruistic gene will spread through a population via kin selection:

$r B - C > 0$

*   **Variables:**
    *    $r$  = Coefficient of relatedness between the actor and the recipient.
    *    $B$  = Fitness benefit conferred upon the recipient (measured in extra offspring produced).
    *    $C$  = Fitness cost incurred by the actor (measured in direct offspring forgone).
*   **Predictions of Hamilton's Rule:**
    *   Altruistic cooperation is favored when relatedness ( $r$ ) is high, benefit ( $B$ ) is large, and cost ( $C$ ) is low.
*   **J.B.S. Haldane's Principle:** Rumored to have stated, "I would jump into a river to save two brothers, but not one. Or to save eight cousins but not seven."
    *   Save 2 brothers:  $2 \times 0.5 = 1.0$ 
    *   Save 8 cousins:  $8 \times 0.125 = 1.0$

Case Study: Coalition Formation in Male Wild Turkeys

Mating System of Wild Turkeys (Meleagris gallopavo):
- Exhibit a lek-like mating system with extreme male-male competition.
- Male turkeys (toms) form cooperative coalitions of $2 \text{ to } 4 \text{ individuals}$ to display to and defend females.
- Within each coalition, only one dominant male performs all copulations; subordinate males display continuously but never mate.

Two Competing Hypotheses (Alan Krakauer):
1. Patient Males Hypothesis: Subordinate males queue for dominance, obtaining direct fitness benefits later in life when the dominant male dies.
2. Kin Selection Hypothesis: Subordinates obtain indirect fitness benefits by helping related dominant males achieve high reproductive success.
Testing Hypothesis Predictions:
- Observational Test: Field studies revealed that coalitions form early in life. If the dominant male dies, subordinate males do not acquire new partners, nor do they ever attain dominance or mate.
- Conclusion: The Patient Males Hypothesis is ruled out.
Quantifying Hamilton's Rule for Turkey Coalitions:
- Genetic Relatedness ( $r$ ): Mean pairwise genetic relatedness between coalition display partners was estimated at $r = 0.42$ (roughly equivalent to full siblings).
- Offspring Production:
  - Dominant males in coalitions fathered an average of $7.0 \text{ offspring}$ .
  - Solo displaying males fathered an average of $0.9 \text{ offspring}$ .
  - Subordinate coalition males fathered $0 \text{ offspring}$ .
- Calculating Benefit ( $B$ ) and Cost ( $C$ ):
  - $\text{Benefit } (B) = \text{Offspring}_{\text{dominant}} - \text{Offspring}_{\text{solo}} = 7.0 - 0.9 = 6.1 \text{ offspring}$
  - $\text{Cost } (C) = \text{Offspring}_{\text{solo}} - \text{Offspring}_{\text{subordinate}} = 0.9 - 0 = 0.9 \text{ offspring}$
- Calculating Net Benefit (Inclusive Fitness Gain):

$\text{Net Benefit} = r B - C$

$\text{Net Benefit} = (0.42 \times 6.1) - 0.9$

$\text{Net Benefit} = 2.562 - 0.9 = 1.662 \text{ offspring}$

*   *Conclusion:* Because  $1.66 > 0$ , Hamilton's rule is satisfied. Subordinate males increase their inclusive fitness more by helping a dominant relative than by displaying solo.

Eusocial Systems and Haplodiploidy

Characteristics of Eusociality:
- Extreme cooperative social organization characterized by:
  1. Overlapping generations.
  2. Cooperative care of young.
  3. Reproductive division of labor (a few breeding individuals, while sterile workers perform all colony maintenance, foraging, and defense).
- Eusociality is observed in bees, ants, wasps, termites, snapping shrimp, and naked mole rats.

Haplodiploid Sex Determination System:
- Present in Hymenoptera (ants, bees, wasps).
- Females develop from fertilized diploid eggs ( $2n$
- Males develop from unfertilized haploid eggs ( $1n$
- Asymmetric Relatedness in Haplodiploidy:
  - Full sisters inherit $100\text{\%}$ of their father's genes and $50\text{\%}$ of their mother's genes.
  - Coefficient of relatedness between full sisters is $r = 0.75$
  - A female's relatedness to her own daughter is $r = 0.5$
  - A female's relatedness to her brother is $r = 0.25$
- Implication: A female haplodiploid insect propagates more of her alleles by rearing sisters ( $r = 0.75$ ) than by producing her own daughters ( $r = 0.5$ ).
Eusociality in Diploid Organisms:
- Although haplodiploidy facilitates kin selection, it is not a strict requirement for eusociality.
- Diploid eusocial groups (e.g., termites, mole rats) achieve high intracolony relatedness through extensive inbreeding and living in isolated, defended central nests.

Coalition Formation in Male Lions and Pika Alarm Calls

Male Lion Coalitions (Panthera leo):
- Male lions form coalitions of $2 \text{ to } 9 \text{ cats}$ to control female harems.
- Only the top two dominant males in a coalition reproduce; lower-ranked males rarely sire cubs.
- In large coalitions ( $3 \text{ to } 4 \text{ males}$ ), lower-ranked males are exclusively close genetic relatives who gain indirect fitness.
- Unrelated male coalitions consist almost exclusively of coalitions of 2 males, where both individuals obtain significant direct fitness benefits by securing dominant breeding ranks.

Percent of Offspring Sired by Male Lion Rank

Territorial Pika Alarm Calls:
- Pikas reside in individual territories where neighbors may or may not be related.
- Support for Benefits Caller Hypothesis: Callers are statistically more likely to avoid predator mortality than non-callers.
- Support for Kin Selection Hypothesis: Calling propensity correlates directly with higher relatedness between callers and immediate neighbors.

Comprehensive Review Questions and Answers

Q5.1: The scenario presented in the cost-benefit analysis of bat blood sharing shows that:
- Answer: Donors give up less time than recipients gain.
Q5.2: If bats only ever play a single game with each other, what is the single best overall strategy?
- Answer: Withhold.
Q5.3: If Buffy shares food, what strategy maximizes your payoff?
- Answer: Withhold food, because $9 > 6$ .
Q5.4: If Buffy withholds food, what strategy maximizes your payoff?
- Answer: Withhold food, because $0 > -3$ .
Q5.5: What is the ESS for the Vampire Bat's Dilemma if played forgetfully?
- Answer: Withhold (a pure ESS).
Q5.6: Which game plan resulted in the highest final fitness score in iterated play?
- Answer: Copy Buffy (Tit-for-Tat).
Q5.7: Which set of conditions is most likely to lead to the evolution of cooperation?
- Answer: Cooperation is more likely to evolve when individuals repeatedly play the same partner and remember that partner's former behavior.
Q5.9: For terrestrial predators, is it true that calling decreases predation risk for caller?
- Answer: No (it doubles mortality risk).
Q5.10: Which sex is more likely to call for terrestrial predators?
- Answer: Females are more likely to call than males.
Q5.11: Do callers discriminate against non-callers during terrestrial attacks?
- Answer: Callers do not discriminate against non-callers.
Q5.12: For aerial predators, is it true that calling decreases predation risk for caller?
- Answer: Yes ( $10\times$ higher escape rate).
Q5.13: Which sex is more likely to call for aerial predators?
- Answer: Males and females are equally likely to call.
Q5.14: Do callers discriminate against non-callers during aerial attacks?
- Answer: Callers do not discriminate against non-callers.
Q5.15: Which hypothesis for ground squirrel trills at terrestrial predators is best supported?
- Answer: Alerts Relatives.
Q5.16: Which hypothesis for ground squirrel whistles at aerial predators is best supported?
- Answer: Benefits Caller.
Q5.17: True or False: A man shares more genes via inheritance with his cousin than he does with his uncle.
- Answer: False (Cousin $r = 0.125$ ; Uncle $r = 0.25$ ).
Q5.18: True or False: A woman shares more genes via inheritance with her daughter than she does with her brother (a full sibling).
- Answer: False (Daughter $r = 0.5$ ; Full Sibling $r = 0.5$ ).
Q5.19: Can you rule out either the Patient Males or Kin Selection hypothesis for wild turkey coalitions?
- Answer: The Patient Males hypothesis can be ruled out.
Q5.20: What does $r = 0.42$ suggest for turkey coalition partners?
- Answer: Coalition partners are about as related as full siblings are.
Q5.21: Calculated values for turkey Hamilton's rule variables:
- Answer: Benefit to dominant male ( $B$ ) = $6.1$ ; Cost to subordinate male ( $C$ ) = $0.9$
Q5.22: What is the Net Benefit (inclusive fitness) subordinate male turkeys expect from helping?
- Answer: $1.66$
Q5.23: True or False: Subordinate male turkeys increase inclusive fitness more by helping dominant males procure mates than by seeking mates on their own.
- Answer: True.
Q5.24: A female leafcutter ant is most likely to improve her inclusive fitness by helping which relative?
- Answer: Her sister ( $r = 0.75$ ).
Q5.25: Which statement is true about eusocial species?
- Answer: Kin selection may help explain the evolution and maintenance of eusociality.
Q5.26: Reciprocity is MOST likely to occur in a species if:
- Answer: Individuals frequently interact with one another.
Q5.27: Wolf scenario (Brother stays and helps sister raise 10 pups vs leaves to father 7 pups; sister surviving pups drops to 5 if he leaves):
- Calculation: Indirect gain from staying = $(10 - 5) \times 0.25 = 1.25$ . Direct gain from leaving = $7 \times 0.5 = 3.5$ . Net Hamilton's rule benefit = $1.25 - 3.5 = -2.25$ .
- Answer: He should leave to seek a mate and father his own litter.
Q5.28: What is the best explanation for why a male lion joins a coalition of unrelated males?
- Answer: Doing so will increase its direct fitness, especially if it is one of the two most dominant males.
Q5.29: Unrelated male lions have the best chance of a fitness benefit in which type of coalition?
- Answer: In a coalition of 2 males.
Q5.30: Which observation provides the best support for the Benefits Caller hypothesis in pikas?
- Answer: Callers are more likely to avoid being killed by predators.
Q5.31: Which observation provides the best support for the Kin Selection hypothesis in pikas?
- Answer: Callers are more closely related to their neighbors than non-callers are.