Chitinase genes (CHIA s) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals

Abstract

The end-Cretaceous extinction led to a massive faunal turnover, with placental mammals radiating in the wake of nonavian dinosaurs. Fossils indicate that Cretaceous stem placentals were generally insectivorous, whereas their earliest Cenozoic descendants occupied a variety of dietary niches. It is hypothesized that this dietary radiation resulted from the opening of niche space, following the extinction of dinosaurian carnivores and herbivores. We provide the first genomic evidence for the occurrence and timing of this dietary radiation in placental mammals. By comparing the genomes of 107 placental mammals, we robustly infer that chitinase genes (CHIAs), encoding enzymes capable of digesting insect exoskeletal chitin, were present as five functional copies in the ancestor of all placental mammals, and the number of functional CHIAs in the genomes of extant species positively correlates with the percentage of invertebrates in their diets. The diverse repertoire of CHIAs in early placental mammals corroborates fossil evidence of insectivory in Cretaceous eutherians, with descendant lineages repeatedly losing CHIAs beginning at the Cretaceous/Paleogene (K/Pg) boundary as they radiated into noninsectivorous niches. Furthermore, the timing of gene loss suggests that interordinal diversification of placental mammals in the Cretaceous predates the dietary radiation in the early Cenozoic, helping to reconcile a long-standing debate between molecular timetrees and the fossil record. 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 numerous chitinase pseudogenes.

Fig. 1. Placental mammal CHIA gene tree, simplified from fig. S3.

Closed circles indicate functional CHIAs, and open circles indicate pseudogenic CHIAs and/or CHIAs lacking a chitinolytic and/or chitin-binding domain. Colored branches correspond to a subset of placental mammal clades: green, Cetartiodactyla; orange, Carnivora; pink, Perissodactyla; red, Xenarthra; purple, Afrotheria; brown, Scandentia; cyan, Strepsirrhini; blue, Anthropoidea; yellow, Dermoptera. Silhouettes and licenses here and throughout are from phylopic.org.

Fig. 2. PGLS regression of the number of functional contig-derived CHIAs versus the percent of the diet consisting of invertebrates.

See text for discussion of highlighted species.

Fig. 3. Examples of CHIA shared inactivating mutations.

Each alignment has a Tarsius syrichta ortholog to provide a functional outgroup comparison. See Fig. 4 for gene inactivations shown in (A) to (M) mapped onto the placental mammal phylogeny.

Fig. 4. Patterns of CHIA loss through time.

(A) The cumulative number of CHIA losses in placental mammals relative to the origin of eutherians, placental mammals, and the K/Pg boundary. Red symbols indicate mean estimates of gene inactivation dates based on four model assumptions, and purple symbols indicate minimum pseudogenization dates based on shared inactivating mutations. Solid bars indicate the range of estimates (table S7), and dashed bars indicate potential range of dates based on branch lengths. (B) The phylogenetic positioning of the CHIA inactivation estimates shown in (A). Letters correspond to gene losses shown in Fig. 3. (C) Timetree (24) indicating lineages sampled for CHIA analyses (red branches). The dashed box indicates zoomed-in portion of phylogeny shown in (B).