Autapomorphic Giantism Associated With Vicariance: A Test of the Island Rule

Aim: When a specific lineage evolves to become significantly larger compared to other lineages in island environments, this can be considered autapomorphic giantism, which follows the island rule. For historical evolutionary events that cannot be reproduced in the laboratory, pattern-based validation is essential to infer the most likely evolutionary processes. This study aimed to test whether the reduction in area due to fragmentation is consistently associated with increased body size in isolated populations, potentially reflecting autapomorphic giantism.

Location: Amami Islands, Ryukyu Islands, Japan.

Taxon: Operculate land snail complex Cyclophorus hirasei hirasei/oshimanus (Caenogastropoda: Cyclophoridae).

Methods: To investigate phylogenetic relationships and population structure within the C. h. hirasei/oshimanus complex, we performed phylogenomic analyses and admixture analyses based on MIG-seq data. Past population dynamics were inferred via approximate Bayesian computation (ABC), and divergence times were estimated using calibrated time-correlated trees. Migration rates among populations were estimated. Shell width variation was analysed using Gaussian mixture models (GMM), and its relationship with environmental factors was tested using phylogenetic generalized linear mixed models (PGLMM).

Results: We detected a repeated association between body size and habitat across genetically distinct populations, even when accounting for phylogenetic relationships (autapomorphic giantism in C. h. hirasei). Parallel evolution in body size occurred among populations on different islands within a short period since the formation of the current islands 2 Ma ago. The migration rate results indicate that the population was extremely sedentary and may have adapted to its habitat independently in each region. Many of the islands were once part of the mainland, and body size may have increased following their isolation due to island formation.

Main Conclusions: Our results demonstrate a spatially replicated pattern of body size divergence that aligns with predictions of the island rule. To our knowledge, this is among the first studies to investigate autapomorphic giantism in terrestrial molluscs from a phylogenomic perspective. These findings highlight Cyclophorus of the Ryukyu Islands as a promising model for studying the predictability of trait evolution and ecological diversification in insular systems.