14Cellulose, a major polysaccharide of the plant cell wall, consists of β-1,4-linked glucose moieties 15 forming a molecular network recalcitrant to enzymatic breakdown. Although cellulose is 16 potentially a rich source of energy, the ability to degrade it is rare in animals and was believed to 17 be present only in cellulolytic microbes. Recently, it has become clear that some animals encode 18 endogenous cellulases belonging to several glycoside hydrolase families (GHs), including GH45. 19GH45s are distributed patchily among the Metazoa and, in insects, are encoded only by the 20 genomes of Phytophaga beetles. This study aims to understand both the enzymatic properties and 21 the evolutionary history of GH45s in these beetles. To this end, we tested the enzymatic abilities 22 of 37 GH45s derived from five species of Phytophaga beetles and learned that beetle-derived 23 GH45s degrade three different substrates: amorphous cellulose, xyloglucan and glucomannan. 24Our phylogenetic and gene structure analyses indicate that at least one gene encoding a putative 25 cellulolytic GH45 was present in the last common ancestor of the Phytophaga, and that GH45 26 xyloglucanases evolved several times independently in these beetles. The most closely related 27 clade to Phytophaga GH45s contained fungal sequences, suggesting this GH family was acquired 28 by horizontal gene transfer from fungi. Other than in insects, arthropod GH45s do not share a 29 common origin and appear to have emerged at least three times independently. 30 31