Not too big, not too small: raids at moderately sized hosts lead to optimal outcomes for a slave-making ant

Abstract

Understanding the trajectory of host-parasite co-evolution requires knowledge of how hosts and parasites impact one another’s fitness, especially among the avian and insect social parasites. Host choice is an important first step in this process, but the principles guiding host choice are unresolved, especially for specialist parasites choosing among individual hosts with multiple traits. To determine how parasites weigh various host traits relative to others, we need to identify their costs and benefits. Here I use the slave-making ant, Temnothorax americanus, to investigate the payoffs from different host trait combinations. I measured the costs and benefits of raids at hosts that varied in their value (# brood), defensive power (# workers), or their ratios. Additionally, I investigated whether slave-maker fighting power influences which host trait combinations were optimal. Slave-makers performed best when hosts contained more brood but fewer workers. However, the ability to maximize this ratio is constrained by the correlation of brood and worker numbers in natural nests, making the optimal host moderately sized. Measures of costs reinforce this conclusion, since slave-maker mortality increased with the number of host workers. Additionally, I found that larger slave-maker colonies have higher payoffs at larger hosts, suggesting their optimal host trait profile differs from smaller colonies. This study shows that social parasites exercising force ought to balance a trade-off between host value and defensibility, rather than maximizing only value. Furthermore, the results highlight that host demography could play a larger role in insect social parasite arms races than previously appreciated. A key to understanding the outcome of co-evolutionary arms races in social parasites is identifying the traits that contribute to the success of parasites and hosts. Host choice determines which traits experience selection, but the relative costs and benefits associated with different host traits, and how parasites ought to weigh them, remains unclear. I measure parasite success in relation to host and parasite demographic traits to distinguish the relative impacts of each using a slave-making ant. Maximizing host brood-to-worker ratio leads to higher payoffs, while the most populous hosts are impenetrable. These findings provide evidence that social parasites attacking by force seek a balance between a host’s value and defensibility, even if it means forgoing hosts with higher potential value. This in turn highlights colony demography and life history as important host traits under selection in co-evolutionary arms races in social insect parasites.