Lecture 28: Helpers at the Nest and the Evolution of Sociality

Negotiation of Family Responsibilities and Evolutionary Conflict

• Timeline of Negotiation: Family responsibilities are negotiated over both ecological and evolutionary timescales.

• Duty Reassignment: Mothers and fathers frequently reassign duties within the family unit.

• Offspring Independence: There is a transition point where offspring begin taking care of themselves.

• Simultaneous Conflicts: Parent-offspring conflict and sexual conflict (between parents) occur at the same time.   - Reference: (Koch and Meunier 2014, Meunier and Kolliker 2012, Thesing et al 2012).

• Adaptation to Loss of Care: Offspring can adapt to the sudden or gradual loss of parental care.   - Reference: (Jarrett et al 2017, 2018, Rebar et al 2019, Schrader et al 2014, 2015, 2017).

Genetic Basis for Mating Systems and Parental Care

• Comparative Study of Voles:   - Prairie Voles: Characterized as monogamous with active male parental care.   - Meadow Voles: Characterized as polygynous with no male parental care.

• Neurobiological Regulation:   - In male Prairie voles, vasopressin and dopamine in the forebrain regulate affiliation and bond formation between mates.   - The expression of the vasopressin receptor is significantly higher in the monogamous Prairie voles compared to the polygynous Meadow voles.

• Experimental Transition (Lim et colleagues):   - Researchers used a viral vector to transfer the vasopressin receptor gene from the Prairie vole into the Meadow vole.   - Result: By changing this single gene, the polygynous Meadow vole became monogamous and the males began to exhibit parental care behaviors.

Theory of Parent-Offspring Conflict

• Trivers (1974): This theory posits that selection acts differently on parents and offspring.

• Fitness Trade-offs: Actions that increase the fitness of the offspring (e.g., more nursing) may simultaneously reduce the fitness of the parent (e.g., reduced ability to produce future offspring).

• Impact of Parental Age:   - Conflict is observed to be higher with younger parents because they still possess high potential for future reproduction.

• Impact of Offspring Age:   - Conflict typically increases as the offspring gets older.   - This occurs because the benefit to the offspring and the cost to the parent ($\text{benefit/cost ratio}$) for continued care decreases.

Helpers at the Nest: Benefits and Characteristics

• Direct Benefits:   - Learning essential skills regarding maternal care.   - Inheriting resources or territories.

• Indirect Benefits (Inclusive Fitness):   - Gaining inclusive fitness by helping related offspring (kin).

• Juvenile Participation:   - In certain species, juveniles remain at the nest to assist with a second nesting effort.   - Sex Bias: Helpers are more frequently female juveniles.   - Species Examples: Voles and Magpie Jays.

Inclusive Fitness and Kin Selection

• The Formula for Inclusive Fitness:   - $\text{Inclusive Fitness} = ext{Direct Fitness (own reproduction)} + ext{Indirect Fitness (relative's reproduction)}$

• Biological Rationale: Individuals share more genes with their relatives than with the general population. Helping relatives allows shared genes to be passed on to future generations.

• Hamilton’s Rule: Cooperation is favored by selection when:   - rB - C > 0   - r > rac{C}{B}   - Where $r = ext{relatedness between altruist and recipient}$.   - Where $B = ext{fitness benefit to the recipient}$.   - Where $C = ext{fitness cost to the altruist}$.   - Attributed to William D. Hamilton ($1936$-$2000$).

• Coefficients of Relatedness ($r$):   - Parent-offspring: $0.5$   - Full siblings: $0.5$   - Half siblings: $0.25$   - Grandparent-grandoffspring: $0.25$   - Step siblings: $0$

Case Studies in Helpers at the Nest

• Pied Kingfishers:   - Primary Helpers: These are offspring of the parents. They deliver more food (fish) and are more closely related to the breeders.   - Secondary Helpers: Less related, providing less assistance.   - Fitness Data (Reyer [964]):     - Primary Helper First Year Indirect Fitness ($f_1$): $1.8 imes 0.32 = 0.58$     - Primary Helper Second Year Direct Fitness ($f_2$): $2.5 imes 0.50 imes 0.54 imes 0.60 = 0.41$     - Delayer First Year Fitness: $0.00$

• Seychelles Warbler (Peter Nash):   - Individuals tend to become helpers only after all high-quality territories are occupied.   - Data from $1988$-$1993$ shows a high percentage of territories with helpers in high-quality areas (e.g., $11$ to $24$) compared to medium-quality areas.

• Florida Scrub Jays (Emlen [359]):   - Experimental removal of helpers showed that nests without helpers had significantly fewer surviving offspring.   - Parental Experience Factor:     - Inexperienced parents without helpers: $1.03$ fledglings.     - Inexperienced parents with helpers: $2.06$ fledglings.     - Experienced parents without helpers: $1.62$ fledglings.     - Experienced parents with helpers: $2.20$ fledglings.   - Indirect Fitness Gained: Primary helpers gain between $0.30$ and $0.60$ in indirect fitness units.

• Cichlid Fish (Neolamprologus pulcher) (Brouwer et al. 2005):   - Helper removal treatment led to a significant decrease in offspring survival (from approx. $90\%$ down to approx. $45\%-50\%$   - Helper Social Behaviors:     - Direct Brood Care: Egg cleaning and substrate cleaning.     - Territory Maintenance: Digging and carrying.     - Other Behaviors: Agonistic behavior and submissive behavior.

Promiscuity and Evolutionary Transitions

• Research by Cornwallis et al.:   - Cooperation is more likely to evolve if the breeding female is monogamous.   - Monogamy/Low Promiscuity: Correlates with high intragroup relatedness and favors the transition to cooperative breeding.   - High Promiscuity: Leads to low intragroup relatedness and independent breeding.   - Data shows that as the number of mates (promiscuity) increases from $2$ to $20$, the relatedness ($r$) drops significantly for both siblings and offspring.

Reproductive Skew and Social Group Dynamics

• Reproductive Skew: The distribution of direct reproduction among cooperating individuals in a group.   - Low Skew: Reproduction is shared equally among members (e.g., Acorn woodpeckers, Prairie dogs).   - High Skew: One or a few individuals dominate reproduction (e.g., Naked mole rats, most ants, bees, yellow jackets).

• Factors Influencing Skew:   - Expected success of breeding independently vs. success within a group.   - Degree of relatedness among group members.   - Probability of a subordinate becoming dominant.   - Individual fighting ability.

• Predictors for Increased Skew:   - Greater ecological constraints on reproducing alone.   - Higher relatedness levels.   - Low individual fighting ability of subordinates.

• Dominant Incentives:   - Staying Incentives: Dominants offer a share of reproduction to ensure subordinates do not leave.   - Peace Incentives: Dominants offer a share of reproduction to reduce aggression from subordinates.

• Example: Dwarf Mongoose (Helogale parvula):   - Groups consist of $7$-$10$ individuals where a dominant pair suppresses subordinate reproduction.   - As individuals age, their dispersal success probability increases. Dominants offer staying incentives specifically to older subordinates to keep the pack strong.

Dispersal and Sociality

• Risks of Dispersal:   - High probability of death.   - Difficulty finding food, shelter, and mates.

• Ecological Constraints: When dispersal costs are high, offspring maximize fitness by staying home, leading to the transition from solitary individuals to social groups.

• Risks of Staying (Non-dispersal):   - Competition with relatives for limited resources.   - Inbreeding depression.   - Conflicts over reproduction.

• Overlapping Generations: This is considered a key step in the evolution of complex sociality.

Evolution of Menopause in Killer Whales (Orcas)

• Life History: Females can live into their $90s$ but stop reproducing in their $30s$ or $40s$.

• Comparison: Humans, pilot whales, and orcas are the only species known to undergo menopause.

• Liability of Losing a Mother:   - Young males are $3$ times more likely to die the year following a mother's death.   - Males over $30$ years old are $8$ times more likely to die without their mother.

• Orca Individual - Granny (J2):   - Estimated lived over $100$ years (died Jan 3, 2017).   - As a post-reproductive matriarch, she guided the pod for foraging, cared for calves, and fed larger males.

• Recent Research (Ellis et al. 2024, Nature):   - Menopause evolved in toothed whales by extending lifespan without extending reproductive lifespan ('live-long' hypothesis).   - This increases the overlap with grandoffspring and offspring for intergenerational help without increasing reproductive competition with daughters.

Summary and Core Concepts

• Helpers at the nest provide both direct (learning/resources) and indirect (kin selection) benefits.

• Helping is tied to overlapping generations and limited dispersal due to territory constraints.

• Inclusive fitness is the sum of direct and indirect fitness components.

• Reproductive skew is influenced by ecological constraints, relatedness, and behavioral incentives.

• Social systems emerge from the balance of costs and benefits associated with group living vs. solitary dispersal.