CE02 - Terre vivante

Evolution of a kin recognition system in social insects – EVOKIN

Submission summary

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Bees, ants and wasps (Hymenoptera) are well known for their ‘eusocial’ lifestyle where queens regulate the reproductive output of up to a million workers. This sacrifice of workers to their colony was a major challenge to the theory of natural selection, acknowledged by Darwin himself. The realisation that helping related individuals indirectly promotes the helper’s overall reproductive success solved part of this evolutionary conundrum. However, this strategy is vulnerable to exploitation by unrelated ‘parasites’. An ability to distinguish kin from non-kin is therefore critical for eusociality to evolve. Given that eusociality is virtually absent in most insect lineages, a major unanswered question is how it was able to evolve nine times in Hymenoptera. Recent studies suggest that eusocial ants possess an olfactory subsystem that is specialized to function in kin recognition, providing a mechanism to detect social parasites. It consists of one type of sensory structure on the antennae, called basiconic sensillae (BaS), which detect cuticular hydrocarbons (CHCs), a blend of chemical cues that can reveal individual’s colony origin. The BaS are connected to a segregated region of the primary olfactory centre in the brain, and are thought to express a group of olfactory receptor (OR) genes with a distinctive 9-exon structure. Strikingly, a similar suite of features has recently been observed in Vespid wasps, which independently evolved a eusocial lifestyle. This suggests that the BaS-subsystem may have played a critical role in the convergent evolution of eusociality by enabling kin recognition. However, we do not know if the BaS-subsystem was present in ancestral solitary species, if it was pre-adapted to support kin-recognition, or how it may have been refined for this task. Answering these questions is central to understanding the striking diversity of social behaviours in Hymenoptera, and to explain why eusociality, normally so rare, has evolved so many times in this clade.

The EVOKIN project proposes an unprecedented endeavour to answer these questions. We will collect data from species representing all major Hymenopteran lineages, a diverse range of social organisations, and multiple independent origins of eusociality. By combining neuroanatomical, chemical and molecular data, together with behavioural and neurophysiological assays, we will test the evolutionary link between the BaS-specific subsystem and eusociality. Specifically, we will:
Aim 1: Reveal how the anatomical organisation of the BaS-specific subsystem varies across Hymenoptera. We will test whether this variation is associated with social organisation, and reconstruct the evolutionary history of key traits across the phylogeny, enabling us to place behavioural and neuronal changes in chronological order.
Aim 2: Use an extensive dataset of OR repertoires across Hymenoptera to test whether 9-exon OR gene number co-evolves with each species’ CHC profile complexity and the number of anatomical units in the BaS-specific subsystem, and examine how transitions in social organisation shape the selection pressures acting on OR genes.
Aim 3: Confirm the function of the BaS-specific subsystem in kin recognition in eusocial lineages, and determine its possible ancestral function in solitary species, by performing behavioural experiments (e.g. dyad encounters) and using in vivo optical imaging to record the neural activity of the BaS-specific subsystem in response to kin, conspecifics, and environmental odours.
Combining detailed neuroanatomical, molecular and functional characterisation of the sensory structures underpinning kin recognition, the EVOKIN project will uncover the neural adaptations that support social behaviour and the remarkable diversity of Hymenopteran social systems.

Project coordination

Jean-Christophe SANDOZ (Évolution, génomes, comportement et écologie)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

LEEC LABORATOIRE D'ÉTHOLOGIE EXPÉRIMENTALE ET COMPARÉE
EBAB University of Bristol / Animal Behaviour and Sensory Biology, School of Biological Sciences
EGCE Évolution, génomes, comportement et écologie

Help of the ANR 528,033 euros
Beginning and duration of the scientific project: December 2020 - 48 Months

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