Helping in cooperatively breeding long-tailed tits: a test of Hamilton's rule

Abstract

Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist (c) are outweighed by the benefit to the recipient (b), weighted by the relatedness of altruist to recipient (r), i.e. Hamilton's rule rb > c. Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton's rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton's condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton's rule for the evolution of altruistic helping behaviour is satisfied in this species.

Keywords: Aegithalos caudatus; altruism; inclusive fitness; kin selection; relatedness; social evolution.

Figure 1.

Adult long-tailed tit showing rings that allow individual recognition in the field. (Online version in colour.)

Figure 2.

Frequency distributions of genetic relatedness of helpers to female breeder (n = 186), male breeder (n = 167) and brood (n = 186) in long-tailed tits. Individuals who were observed to provision a nest only once were excluded. Estimates were made using molecular markers (see [44] for details of genotyping methods).

Figure 3.

Probability of recruitment for male fledgling long-tailed tits in relation to the number of helpers that provisioned them as nestlings. Circles show the observed proportions of recruited males for each number of helpers, scaled by sample size. Solid line shows model fitted probability of recruitment for males from a multilevel logistic regression [58] on data for males and females (n = 1242; males = 672). The model had fixed effects for sex and number of helpers and random effects for year (1994–2009, excluding 2001) and nest ID (163 nests). The fixed part of the model was logit⁻¹(−1.57–0.99 × female + 0.32 × helpers). Dotted lines show 95% confidence intervals calculated from simulations of the posterior distribution of each model parameter [59].

Figure 4.

The probability of renesting following the failure of a breeding attempt in relation to standardized date of the breeding season for males that became helpers and males that did not become helpers. Failure dates and helping/renesting behaviour of breeders were recorded in the Rivelin Valley population over 18 years (1995–2013, with 2001 excluded). We excluded pairs that failed before the median lay date of first attempts in that year. In each year, we estimated ‘termination date’ as the date when 50% of females were expected to give up breeding, by modelling female renesting versus termination as a function of failure date in a series of annual logistic regressions (see [80] for full methods). We then calculated ‘relative failure date’ of breeding males as absolute failure date minus termination date in that year, plus 100 to remove negative values. This ‘relative failure date’ was calculated for all breeding males with known ID (n = 377). We split the 868 nests belonging to these males into two subsets depending on their behaviour following nest failure: those that eventually went on to help at a nest of another bird in that year (n = 413), and those that did not help after failing but instead terminated breeding for that year (n = 455). We then modelled the probability of males renesting versus terminating breeding, in response to relative failure date, using a binomial model with logit link function. We repeated this for helpers and non-helpers separately. The overall mean inflection point (50% probability of renesting) was 96.7 days ± 0.65 s.e. and did not differ for males that became helpers (97.2 ± 0.93 s.e.) and non-helpers (96.2 ± 0.91 s.e.).