Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus

Abstract

In Pogonomyrmex californicus harvester ants, an age-associated division of labor occurs in the worker caste, in which young workers perform in-nest tasks and older workers forage for food. Here, we tested whether this behavioral division is age based or age flexible, and whether it coincides with differential expression of systemic hormones with known roles in behavioral regulation. Whole-body content of juvenile hormone (JH) and ecdysteroids was determined in workers from (1) age-typical colonies, in which a typical age structure is maintained and workers transition across behaviors naturally, and (2) single-cohort colonies, which are entirely composed of same-aged workers, facilitating the establishment of age-independent division of labor. Foragers from both colony types had higher JH and lower ecdysteroid content than workers performing in-nest tasks, suggesting that age is not the sole determinant of worker behavior. This association between hormone content and behavior of P. californicus workers is similar to that previously observed in founding queens of this species. Because these hormones are key regulators of development and reproductive behavior, our data are consistent with the reproductive ground plan hypothesis (RGPH), which posits that the reproductive regulatory mechanisms of solitary ancestors were co-opted to regulate worker behavior.

Fig. 1.

Age of confirmed foraging of age-typical and single-cohort colonies. Single-cohort workers initiated foraging significantly earlier, as indicated by the asterisk (Mann-Whitney U-test, P<0.05). Sample sizes are indicated above the bars.

Fig. 2.

Mean ± s.e.m. content (pg ant^-1) of juvenile hormone (JH) and ecdysteroids of (A) age-typical workers transitioning naturally from nest (N) to foraging (F) stages, and (B) single-cohort workers performing nest (N) or foraging (F) tasks. Significant differences in juvenile hormone and ecdysteriod content between nurses and foragers are indicated by asterisks and daggers, respectively. Age-typical ecdysteroids: Student's t-test, P<0.05; all others: Mann-Whitney U-test, P<0.05 between groups. In addition, JH content of single-cohort foragers is significantly higher than JH content of age-typical foragers (Mann-Whitney U-test, P<0.05). For both the age-typical (C) and single-cohort (D) colonies, each component colony has too low a sample size for robust statistical analyses; however, the general trend in each colony is the same as the overall result (A and B, respectively). Sample sizes are indicated above the bars.

Fig. 3.

Scatter plot showing distribution of hormone content in relation to age. There is a significant positive association between JH content and age in age-typical colonies (A), but no such correlation exists for single-cohort colonies (B). Similarly, a significant negative correlation is observed between ecdysteroid content and age in age-typical colonies (C), but not in single-cohort colonies (D). This relationship illustrates that the association between hormone content and behavior is not necessarily age associated, as the relationship disappears in single-cohort colonies. Asterisks denote significant correlations, and Spearman coefficients (ρ) are indicated (Spearman rank correlation, P<0.05).

Fig. 4.

A summary of the hypothesized relationship between JH, ecdysteroids, age and division of labor in P. californicus workers. Age is defined as the age of any given worker cohort, from adult emergence until death. That is, as a group of workers age (x-axis), the proportion of workers performing different tasks changes (y-axis). High JH content corresponds to foraging activities, and a high ecdysteroid content with nest tasks; the bisecting line represents the proportion of workers performing nurse (blue) or foraging (yellow) tasks, and demarks the different hormone levels. (A) In age-typical colonies, the vast majority of young workers have low JH levels and high ecdysteroid levels, and are inside the nest performing nursing tasks. As they age, more workers initiate foraging, which is a behavioral transition that is associated with high JH and low ecdysteroids. (B) In single-cohort colonies, foraging onset begins at a much earlier age, and proceeds faster, until the colony has achieved the necessary balance between nurses and foragers. In both colony types, the onset of foraging coincides with increased JH and decreased ecdysteroid levels.