Reversible plasticity in brain size, behaviour and physiology characterizes caste transitions in a socially flexible ant (Harpegnathos saltator)

Abstract

Phenotypic plasticity allows organisms to respond to changing environments throughout their lifetime, but these changes are rarely reversible. Exceptions occur in relatively long-lived vertebrate species that exhibit seasonal plasticity in brain size, although similar changes have not been identified in short-lived species, such as insects. Here, we investigate brain plasticity in reproductive workers of the ant Harpegnathos saltator. Unlike most ant species, workers of H. saltator are capable of sexual reproduction, and they compete in a dominance tournament to establish a group of reproductive workers, termed 'gamergates'. We demonstrated that, compared to foragers, gamergates exhibited a 19% reduction in brain volume in addition to significant differences in behaviour, ovarian status, venom production, cuticular hydrocarbon profile, and expression profiles of related genes. In experimentally manipulated gamergates, 6-8 weeks after being reverted back to non-reproductive status their phenotypes shifted to the forager phenotype across all traits we measured, including brain volume, a trait in which changes were previously shown to be irreversible in honeybees and Drosophila. Brain plasticity in H. saltator is therefore more similar to that found in some long-lived vertebrates that display reversible changes in brain volume throughout their lifetimes.

Keywords: Harpegnathos; brain plasticity; cuticular hydrocarbons; reproduction; social insects; venom production.

Figure 1.

Changes in behaviour. (a) Proportion of observations (median, 25–75%, and non-outlier range) when control and reverted gamergates were in the foraging arena outside the nest. (b) Proportion of control and reverted gamergates that stung and subdued a cricket, (c) opened their mandibles when provoked with forceps, and (d) bit and stung forceps when provoked. Asterisks indicate significant differences (p < 0.001). (Online version in colour.)

Figure 2.

Cuticular hydrocarbon profiles. (a) Example cuticular hydrocarbon profiles of a control gamergate, reverted gamergate, inside worker, and forager (shaded area indicates the reproductive-associated compound 13,23-dimethylheptatriacontane). Non-reproductive workers and reverted gamergates exhibit intracolonial profile variation typical in this species [22]. (b) Relative proportion of 13,23-dimethylheptatriacontane present in the cuticular profiles of all roles (median, 25–75%, and non-outlier range). Letters indicate significant differences between roles (p < 0.0001; electronic supplementary material, table S3). (Online version in colour.)

Figure 3.

Changes in internal anatomy. (a) Number of yolky oocytes present in the ovaries and (b) venom sac volume of control gamergates, reverted gamergates, inside workers, and foragers (median, 25–75%, and non-outlier range). Letters indicate significant differences between roles (p < 0.05; electronic supplementary material, table S3). (Online version in colour.)

Figure 4.

Changes in brain volume. (a) Total brain volume of control gamergates, reverted gamergates, inside workers, and foragers 6–8 weeks after reintroduction. (b) Brain regions (OL, optic lobes; AL, antennal lobes; and CB, central brain) shown on two-dimensional section of scanned H. saltator brain; (c) central brain, (d) optic lobe, and (e) antennal lobe volume of control gamergates, reverted gamergates, inside workers, and foragers (median, 25–75%, and non-outlier range). Letters indicate significant differences between roles (p < 0.05; electronic supplementary material, table S3). (Online version in colour.)

Figure 5.

Gene expression changes. (a) Vitellogenin (Vg) and (b) Elongase (ELOV) expression relative to GAPDH of control gamergates, reverted gamergates, inside workers, and foragers (median, 25–75%, and non-outlier range). Letters indicate significant differences between roles (p < 0.0001; electronic supplementary material, table S3). (Online version in colour.)

Figure 6.

Correlated plasticity in brain, behaviour, and physiology between reproductive and non-reproductive workers. (Online version in colour.)