Comparative analyses of micro- and macro-scale surface structures in the convergent evolution of rain-harvesting behaviour in lizards

Rain-harvesting behaviour represents an adaptation for water collection that has evolved in some species of iguanian reptiles inhabiting arid environments. To date, such behaviour has been observed only in members of the families Agamidae and Phrynosomatidae. A common set of integumentary features characterizes these rain-harvesting species, including scale surface microstructures (SSMs), capillary channels and hinge joints. The influence of variations in these features on rain-harvesting has been a subject of discussion for many decades. Nevertheless, a comprehensive comparative study of similarities and differences between harvesting and non-harvesting species on a broader scale remains lacking. In this study, we classify scale surface microstructures into three categories: large hexagons (SSM1), smaller nested hexagons (SSM2) and hinge pits (SSM2H). As the first two SSM types are widespread, they do not appear to be directly linked to the adaptation for rain-harvesting. Conversely, the presence or absence of hinge pits distinguishes harvesters from non-harvesters. Additionally, channel hierarchy, width and structure determine the effectiveness of the rain-harvesting architecture. Only Moloch horridus exhibits distinct integumentary features in comparison to other agamids and rain-harvesting species. Ancestral character state reconstruction suggests that rain-harvesting behaviour was likely absent in the ancestor of Iguanians, even though overlapping scales and SSM1 were present. Our findings illustrate that rain-harvesting species have independently converged upon similar structural solutions to address their water acquisition challenges, building upon shared pre-existing features.