Complexity shapes uniqueness: Neuropil volumes and synaptic clusters shape behavioural plasticity under challenging environments in the invasive Argentine ants

Adaptation to new environments is key for organisms’ survival, but also for their invasiveness in their introduced areas. Behaviour is considered the fastest phenotype allowing adaptation, but its plasticity can involve costs as neural development. Although individuals’ investment in cognition was pointed out as unnecessary for colony behaviour in eusocial insects, recent studies are highlighting the behavioural dependence on neural traits in eusocial insects. The costs of producing behavioural and neural plastic offspring could exceed the investments of eusocial insects, in which one or certain reproductives must produce multiple offspring. Thus, we wanted to analyse the link between the neuroanatomy and the behavioural variability of Linepithema humile , an invasive species organised in supercolony units containing millions of individuals, to understand its adaptive mechanisms. We repeatedly tested same aged callow workers of L. humile in behavioural tests of increasing environmental complexity and analysed the volume of their brain functional areas (neuropils) and the synaptic clusters abundance in the mushroom body calices (information processing). Given the potential large cost of plasticity, we expected to find homogeneous interindividual neuronal structures and behavioural responses. Although L. humile is considered a monomorphic species, body size conditioned behavioural and neural traits and determined individuals efficiency in exploring simple environments. Contrary to our expectations, the increase in environmental complexity revealed the behavioural plasticity of Linepithema humile workers as well as its correlation with neuropil volumes and synaptic clusters. Our results highlight the relevance of the central complex and the mushroom bodies on exploration efficiency rather than optic and olfactory lobes. Behavioural plasticity under complex environments relied on the synaptic connections of the olfactory processing area (dense lip), while individuals with higher number of synaptic connections on the visual processing area (collar) explored complex environments less efficiently. Our results suggest that behavioural differences that correlate with morphological traits might promote adaptive mechanisms in simple environments, whereas neurologically based plastic behavior may be necessary to adapt in complex environments.