Sexual dimorphism divergence between sister species is associated with a switch in habitat use and mating system in thorny devil stick insects

•Male thorny devil stick insects are unusually large for male stick insects.•They also display larger and more armoured hindlegs than females.•This lineage switched from solitary roosting in the canopy to aggregating inside cavities.•This switch is associated with a change in their mating system from a searching to a defense polygyny.•Males use their enlarged hindlegs in male competition for access to females. The habitat and resource use of females critically affects their pattern of distribution and consequently their monoposibility by males and the mating system of a species. Shifts in habitat use are therefore likely to be associated with changes in mating system and sexual selection acting on males’ phenotypes, consequently affecting patterns of sexual dimorphism. Although sexual dimorphism is often correlated with shifts in habitat use at the macroevolutionary scale, the underlying microevolutionary processes involved are typically unclear. Here, we used the New Guinean stick insect genus Eurycantha to investigate how changes in habitat use and mating system were associated with a change in sexual dimorphism seen specifically in the thorny devil stick insects (Eurycantha calcarata and Eurycantha horrida). Male thorny devils display sexually dimorphic and enlarged hindlegs endowed with a sharp spine. Sexual size dimorphism is also very reduced in these species relative to other phasmids. Using field observations, morphological measurements and radiotelemetry, we investigated changes in mating system associated with the reduction of sexual dimorphism and tested predictions from the hypothesis that sexual selection drove the evolution of this unusual male morphology. We found that thorny devils switched from solitary roosting in the canopy during the day to communal roosting inside cavities of a few host trees, shifting the distribution of females from scattered to clumped. Male thorny devils used their large hindlegs to fight with rivals for positions on the tree close to cavities containing females, and larger males were associated with cavities containing relatively more females. In contrast, the sister species, Eurycantha insularis, displays relatively small and unarmoured males (ancestral state). Adult female E. insularis were always scattered in the canopy, and this species displayed a scramble competition mating system typical of other phasmids, where mobility, rather than fighting ability, is probably critical to males’ reproductive success. Ove