Intergenerational genotypic interactions drive collective behavioural cycles in a social insect

Abstract

Many social animals display collective activity cycles based on synchronous behavioural oscillations across group members. A classic example is the colony cycle of army ants, where thousands of individuals undergo stereotypical biphasic behavioural cycles of about one month. Cycle phases coincide with brood developmental stages, but the regulation of this cycle is otherwise poorly understood. Here, we probe the regulation of cycle duration through interactions between brood and workers in an experimentally amenable army ant relative, the clonal raider ant. We first establish that cycle length varies across clonal lineages using long-term monitoring data. We then investigate the putative sources and impacts of this variation in a cross-fostering experiment with four lineages combining developmental, morphological and automated behavioural tracking analyses. We show that cycle length variation stems from variation in the duration of the larval developmental stage, and that this stage can be prolonged not only by the clonal lineage of brood (direct genetic effects), but also of the workers (indirect genetic effects). We find similar indirect effects of worker line on brood adult size and, conversely (but more surprisingly), indirect genetic effects of the brood on worker behaviour (walking speed and time spent in the nest).

Division of labour underlies efficient colony defence in a clonal ant

“…This detected the position of each ant every 50 ms. Raw tracking data underwent preprocessing in MATLAB (R2023b) to identify missing or aberrant positions, which were then interpolated or removed, respectively, following Jud et al 2022.…”

“…This detected the position of each ant every 50 ms. Raw tracking data underwent preprocessing in MATLAB (R2023b) to identify missing or aberrant positions, which were then interpolated or removed, respectively, following Jud et al 2022. In each trial, we used BORIS (Friard and Gamba 2016) to manually annotate behaviour in the first 20 min after the introduction of the intruder. We annotated encounters of all clonal raider ants (individually identifiable by their unique paint marks) with the intruder as well as their defence behaviour towards the intruder.…”

Behavioural individuality determines infection risk in clonal ant colonies

“…Synchronised reproduction drives stereotypical colony cycles lasting ca. 5 weeks 52 , in which colonies alternate between reproductive and brood-care phases, corresponding to the absence and presence of larvae, respectively. During the reproductive phase, all ants remain in the nest and lay eggs.…”

Behavioural individuality determines infection risk in clonal ant colonies

“…Synchronized reproduction drives stereotypical colony cycles lasting ca. 5 weeks 47 , in which colonies alternate between reproductive and brood-care phases, corresponding to the absence and presence of larvae, respectively. During the reproductive phase, all ants remain in the nest and lay eggs.…”

“…Individual trajectories were extracted from videos using the software anTraX 64 . Extranidal activity, defined as the fraction of time an ant was outside the nest, was computed using MATLAB v.2022a (MathWorks, Natick, MA, USA) following Jud et al 47 .…”