Group augmentation underlies the evolution of complex sociality in the face of environmental instability

Abstract

Although kin selection is assumed to underlie the evolution of sociality, many vertebrates-including nearly half of all cooperatively breeding birds-form groups that also include unrelated individuals. Theory predicts that despite reducing kin structure, immigration of unrelated individuals into groups can provide direct, group augmentation benefits, particularly when offspring recruitment is insufficient for group persistence. Using population dynamic modeling and analysis of long-term data, we provide clear empirical evidence of group augmentation benefits favoring the evolution and maintenance of complex societies with low kin structure and multiple reproductives. We show that in the superb starling (Lamprotornis superbus)-a plural cooperative breeder that forms large groups with multiple breeding pairs, and related and unrelated nonbreeders of both sexes-offspring recruitment alone cannot prevent group extinction, especially in smaller groups. Further, smaller groups, which stand to benefit more from immigration, exhibit lower reproductive skew for immigrants, suggesting that reproductive opportunities as joining incentives lead to plural breeding. Yet, despite a greater likelihood of becoming a breeder in smaller groups, immigrants are more likely to join larger groups where they experience increased survivorship and greater reproductive success as breeders. Moreover, immigrants form additional breeding pairs, increasing future offspring recruitment into the group and guarding against complete reproductive failure in the face of environmental instability and high nest predation. Thus, plural breeding likely evolves because the benefits of group augmentation by immigrants generate a positive feedback loop that maintains societies with low and mixed kinship, large group sizes, and multiple reproductives.

Keywords: cooperative breeding; direct benefits; group augmentation; plural breeding; social evolution.

Fig. 1.

Simulations of discrete time population growth models show the effects of immigration and starting group size on the extinction risk of superb starling social groups. (A) The results of 100 simulations of a discrete time population growth model (purple = simulation trajectories that resulted in group extinction, blue = simulation trajectories that did not lead to group extinction) overlaid with longitudinal data from nine social groups (black). With immigration set to zero, over half of all iterations (61%) resulted in group extinction in 29 time-steps. However, (B) with immigration, only 18% of the iterations resulted in group extinction over the same time period. Thus, immigration increases the persistence of superb starling social groups. (C) Larger groups are more stable over time. With a larger starting group size (x axis), the percentage of groups going extinct over 29 time-steps (y axis) decreased (Z = −21.93, P < 0.001) (black points). However, when the relationship between immigration and group size was reversed artificially, the percentage of groups going extinct approaches or falls to zero (N₀10: mean ± SD = 1 ± 0.5%; N₀20: 0 ± 0%; N₀30: 0 ± 0% of iterations resulting in group extinction) and does not vary with variation in starting group size (gray points), indicating that in this scenario, immigration compensates for lower offspring recruitment in smaller groups (SI Appendix).

Fig. 2.

Inverse density dependence, or Allee effects, in superb starling social groups. Smaller groups fledged fewer offspring in a breeding season than larger groups (N = 255, group size: Z = 4.51, P < 0.001; group size²: Z = −1.94, P = 0.05), and those below the group size threshold of seven individuals (dotted red line) never fledged any offspring. Points indicate raw data slightly jittered horizontally to improve visual discrimination. Solid line indicates model fit bounded by 95% CIs in light gray.

Fig. 3.

Reproductive skew, likelihood of immigration, reproductive fitness outcomes, and group augmentation benefits of immigrants in superb starling social groups. (A) The sharing of reproductive opportunities was more equitable for both sexes (all males = black, open circles, dashed line; immigrant males only = blue, closed circles, solid line; immigrant females = red, closed triangles, solid line) in smaller groups and in very large groups (SI Appendix). Moreover, in males, the effect size was larger for immigrants only than that for all males. However, (B) immigrants of both sexes were more likely to join larger groups where they were able to (C) nest more times per breeding season and thus (D) accrue higher reproductive success. In contrast, resident males (orange, open circles, dashed lines) did not nest more times per breeding season in larger groups, and the number of nesting attempts did not affect their likelihood of reproductive success in a breeding season, suggesting that they employ an alternative reproductive strategy and are thus likely not negatively impacted by immigrant males breeding within the same social group. Additionally, (E) with more breeding pairs in a group, the likelihood of at least one breeding male being an immigrant increased, despite the presence of more than enough reproductively capable resident males (SI Appendix). (F) While fewer breeding pairs were enough to ensure reproductive success for the group as a whole in benign environmental conditions (dark green, open circles = higher than mean rainfall), more breeding pairs were needed to collectively insure the group against complete reproductive failure in harsh environmental conditions (light green, closed circles = lower than mean rainfall). Points indicate raw data slightly jittered horizontally to improve visual discrimination. Lines indicate model fits surrounded by 95% CIs in light gray.

Fig. 4.

Conceptual framework of direct and indirect group augmentation benefits driving formation and maintenance of social groups with complex group structure in superb starlings. (A) Immigrants (blue) directly augment the size of a group by increasing the number of group members. (B) Some of the immigrant males acquire breeding positions in the group alongside residents (yellow), increasing the number of breeding pairs (indicated as “br”) and consequently the likelihood of reproductive success for the group as a whole, which (C) indirectly augments the size of the group by increasing the number of future group members. (D) Larger groups attract more immigrants, creating a positive feedback loop that maintains immigration and plural breeding, despite the accompanying decline in group kin structure, in superb starling societies.