Evolutionary transitions of complex labile traits: Silk weaving and arboreal nesting in Polyrhachis ants

Understanding the maintenance and evolution of complex group behavioural systems has broad significance to our understanding of social evolution, yet we have little insight into how these systems have evolved. Nest-weaving, a rare group behaviour considered a pinnacle of cooperative action in social insects, involves the coordination of workers and larvae by incorporating larval silk into the nest structure. To investigate the evolution of this complex behaviour in the ant genus Polyrhachis, we used comparative analysis and an inferred molecular phylogeny based on three mitochondrial genes COI, COII and CytB, and three nuclear genes EF1 a-F2, Wg and Tf. Our results showed that arboreality and nest-weaving are closely associated, but in contrast to the previous hypotheses, represent the ancestral state in the monophyletic genus. Nest-weaving within the genus, moreover, is remarkably labile. Arboreality and nest-weaving have been lost and partially regained on at least two occasions: two non-weaving subterranean species (sister taxa likely reflecting a single evolutionary event) have reverted to arboreal nesting habits without regaining the use of silk nests, while a third subterranean species has transitioned to nesting in silk nests on the sides of rocks, obtaining silk from spiders and not their own larvae. The loss of larval cocoons, which is correlated with the most complex form of nest-weaving behavior as typified in Oecophylla, has occurred independently on at least two occasions within Polyrhachis. The repeated loss of nest-weaving behaviour and its partial regaining within the genus provides the first example of a complex group-level trait that did not arise through behavioural progression from simple to complex states. The evolution and loss of complex group-level traits may be more evolutionarily labile than previously appreciated.