Low relatedness can drive the evolution of reproductive division of labour
by Dominic K. Devlin | Austen R.D. Ganley | Nobuto Takeuchi | The University of Auckland | The University of Auckland | The University of Auckland
Abstract ID: 71
Event: The 3rd AsiaEvo Conference
Topic: Open category
Presenter Name: Nobuto Takeuchi

Reproductive division of labour (RDL), where sterile 'helpers' assist specialised 'reproducers' in transmitting genetic information, has evolved repeatedly and at vastly different biological scales. Examples include eusocial insects with queens and workers, multicellular organisms with germline and soma cells, and cells with genomes and enzymes (enzymes provide catalysis, 'helping' genomes transmit genetic information). This recurrent evolution of RDL poses an apparent paradox to the theory of natural selection: helpers sacrifice their own reproduction to perform functions beneficial to a group, but such altruists are susceptible to invasion by 'cheaters'—selfish individuals that avoid cooperation and maximise their own fitness to the detriment of the group. The classical approach to resolve this paradox is through kin selection: altruism can be selected if individuals within groups are genetically related. Under this theory, high relatedness is an essential driver for the evolution of RDL. Here, we demonstrate the converse scenario that low relatedness drives the evolution of RDL. We hypothesise that RDL can function to protect a group against the evolution of cheaters by limiting the transmission of genetic information to a small number of reproducers per group (e.g., genomes, germline cells, and queens), thereby increasing relatedness within groups. Under this hypothesis, RDL is more likely to evolve for lower relatedness because the protective benefit of RDL amplifies as the risk of cheater evolution heightens. To test this prediction, we investigate an agent-based model in which individuals are partitioned into groups that reproduce. Each individual invests a fraction of its resources in self-reproduction and the remainder in the provision of a public good required for the reproduction of individuals in its group. An individual's reproduction is tied to the group's reproduction because a group splits if the number of individuals in the group exceeds a constant threshold. This creates a conflict: greater investment in public-good provision is advantageous for a group but disadvantageous for an individual, as it diminishes that individual's reproduction rate relative to other individuals within the same group. Our results show that individuals within a group differentiate through evolution into two types: reproducers, which invest all their resources in reproduction, and helpers, which invest a large fraction of their resources in public-good provision and do not transmit genetic information across generations—hence, the evolution of RDL. Critically, this evolution occurs only if the average number of individuals per group is sufficiently large, a condition that implies large genetic variation within groups, i.e., low relatedness, as predicted by our hypothesis. Finally, we find that RDL elevates relatedness within a group, stabilising a group against fitness decay caused by cheater evolution. Therefore, the evolution of RDL is a cause, rather than a consequence, of high relatedness in our model. Taken together, our findings provide a novel perspective in evolutionary theory by revealing that the evolution of RDL can be driven by protection against cheaters, with this benefit occurring only if relatedness is sufficiently low.