Convergent evolution of an extreme dietary specialisation, the olfactory system of worm-eating rodents

International audienceTurbinal bones are key components of the mammalian rostrum that contribute to three critical functions: (1) homeothermy, (2) water conservation and (3) olfaction. With over 700 extant species, murine rodents (Murinae) are the most species-rich mammalian subfamily, with most of that diversity residing in the Indo-Australian Archipelago. Their evolutionary history includes several cases of putative, but untested ecomorphological convergence, especially with traits related to diet. Among the most spectacular rodent ecomorphs are the vermivores which independently evolved in several island systems. We used 3D CT-scans (N = 87) of murine turbinal bones to quantify olfactory capacities as well as heat or water conservation adaptations. We obtained similar results from an existing 2D complexity method and two new 3D methodologies that quantify bone complexity. Using comparative phylogenetic methods, we identified a significant convergent signal in the rostral morphology within the highly specialised vermivores. Vermivorous species have significantly larger and more complex olfactory turbinals than do carnivores and omnivores. Increased olfactory capacities may be a major adaptive feature facilitating rats' capacity to prey on elusive earthworms. The narrow snout that characterises vermivores exhibits significantly reduced respiratory turbinals, which may reduce their heat and water conservation capacities. Understanding how species have adapted to their environment is a major goal of evolutionary biology 1-3. Salient examples of convergence, the evolution of a similar trait in independent evolutionary lineages 4 , have demonstrated the importance of determinism through natural selection 3. Recent advances in X-ray microtomography (X-ray µCT) provide the opportunity to quantify convergence in morphological structures that are otherwise inaccessible 5-7. In mammals, the use of morphological proxies such as inner ears, braincase, floccular fossa, cribriform plate, and turbinal bones 5-11 have shed light on ecological and functional adaptations, especially for taxa that are difficult to observe directly in the wild 7. Extensive studies of the mammalian olfactory subgenome revealed that mammals have a wide array of olfactory receptor genes that represent 1-6% of their genomes 12-14. The huge mammalian olfactory subgenome has proven useful to illustrate dietary and other adaptions 12,15,16. However, the nasal chamber of mammals has been relatively neglected by anatomists due to its internal position 17 , and few studies have tested for an adaptive link between nasal morphology and olfactory capacities 18-20