Mammalian chitinase (CHIA) genes provide genomic signal of post-Cretaceous/Paleogene adaptive radiation in placental mammalsAbstract:
The end-Cretaceous extinction led to a massive faunal turnover, with placental mammals radiating following the demise of non-avian dinosaurs. Fossils indicate that Cretaceous stem placentals were generally insectivorous, whereas their Cenozoic descendants occupied a variety of dietary niches, following the extinction of dinosaurian carnivores and herbivores. Despite evidence of these dietary shifts in the fossil record, genomic data have yet to provide evidence for this hypothesis. Here we show that CHIA genes, encoding chitinases capable of digesting insect exoskeletal chitin, were repeatedly lost as placental mammals radiated into non-insectivorous lineages. Comparing the genomes of 107 placental mammals, we found that CHIA, previously thought to be a single copy gene, was present as five paralogs in the ancestral placentalian. As placental mammals radiated near the Cretaceous/Paleogene boundary, multiple CHIA copies were convergently inactivated, particularly in non-insectivorous lineages, leading to a positive correlation between the amount of invertebrates ingested and the number of intact CHIA genomic copies. Furthermore, we provide evidence that the timing of CHIA loss is consistent with a long-fuse model of placental mammal evolution. Our results demonstrate that placental mammal genomes, including humans, retain a molecular record of the post-K/Pg placental adaptive radiation in the form of chitinase pseudogenes.