A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae)

The Palaearctic genus Arvicola includes two species: the south‐western water vole A. sapidus, and the northern water vole A. terrestris. The latter has semiaquatic and/or subterranean populations, while populations of A. sapidus are always semiaquatic. According to the current phylogenetic and palaeontological data, adaptation to semiaquatic life is plesiomorphic for the genus Arvicola. We studied the ontogenetic allometry of skull and long bones of the semiaquatic A. sapidus, a semiaquatic population of A. terrestris (A. t. italicus), and two fossorial populations of A. terrestris (A. t. scherman and A. t. monticola). Animals from fossorial populations were smaller than were those from semiaquatic populations. We found that most of the ontogenetic allometric exponents of characters linked to digging in the skull and in the long bones were significantly higher in A. t. monticola, a fossorial clade, than they were in the semiaquatic populations. On the other hand, there may have been an evolutionary lag between invasion of the hypogeic habitat and the acquisition of fossorial adaptations in A. t. scherman. We showed statistically that the morphological differences linked to the invasion of a hypogeic habitat are already present in juvenile animals and, according to these results, suggest that these morphological differences are the direct expression of genetic changes rather than the outcome of epigenetic factors of mechanical origin. Moreover, we tried to ascertain whether the apomorphic shape of the skull and long bones in the fossorial populations of A. terrestris (compared with the primitive condition that would have been retained by the semiaquatic A. sapidus) are the outcome of a heterochronic process. Optimization by squared change parsimony supported the hypothesis of an apomorphic reduction of body size linked to the invasion of the subterranean habitat. The comparison of the ontogenetic trajectories of both skull shape and long bone shape suggested that a heterochronic process was involved in this morphological transformation. By using the ‘clock model’ method, this mechanism was identified as ‘accelerated dwarfism’ affecting both the skull and long bones. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87 , 381–391.