The giant pouched rat (Cricetomys ansorgei) olfactory receptor repertoire

Abstract

For rodents, olfaction is essential for locating food, recognizing mates and competitors, avoiding predators, and navigating their environment. It is thought that rodents may have expanded olfactory receptor repertoires in order to specialize in olfactory behavior. Despite being the largest clade of mammals and depending on olfaction relatively little work has documented olfactory repertoires outside of conventional laboratory species. Here we report the olfactory receptor repertoire of the African giant pouched rat (Cricetomys ansorgei), a Muroid rodent distantly related to mice and rats. The African giant pouched rat is notable for its large cortex and olfactory bulbs relative to its body size compared to other sympatric rodents, which suggests anatomical elaboration of olfactory capabilities. We hypothesized that in addition to anatomical elaboration for olfaction, these pouched rats might also have an expanded olfactory receptor repertoire to enable their olfactory behavior. We examined the composition of the olfactory receptor repertoire to better understand how their sensory capabilities have evolved. We identified 1145 intact olfactory genes, and 260 additional pseudogenes within 301 subfamilies from the African giant pouched rat genome. This repertoire is similar to mice and rats in terms of size, pseudogene percentage and number of subfamilies. Analyses of olfactory receptor gene trees revealed that the pouched rat has 6 expansions in different subfamilies compared to mice, rats and squirrels. We identified 81 orthologous genes conserved among 4 rodent species and an additional 147 conserved genes within the Muroid rodents. The orthologous genes shared within Muroidea suggests that there may be a conserved Muroid-specific olfactory receptor repertoire. We also note that the description of this repertoire can serve as a complement to other studies of rodent olfaction, as the pouched rat is an outgroup within Muroidea. Thus, our data suggest that African giant pouched rats are capable of both natural and trained olfactory behaviors with a typical Muriod olfactory receptor repertoire.

Fig 1. Phylogeny of species compared in this study.

The figure shows a simplified phylogeny of mice (Mus sp.), rats (Rattus sp.), pouched rats (Cricetomys sp.), and squirrels (Ictidomys sp.). Pouched rats are Nesomyid rodents that are distantly related to Murids. Silhouettes show approximate size differences among species. Time periods are listed along the x-axis, and estimated from previous research [31,32,39]. MYA: million years ago, Plioc: Pliocene, IV: Quaternary period.

Fig 2. Family-group representation in the pouched rat olfactory receptor gene tree.

Different colors at nodes indicate different families. Colors are repeated within the tree, but similar colors do not indicate similarity of families. All families share > 50% bootstrap support and 40% protein identity.

Fig 3. Graph comparing functional and pseudogene numbers among select species.

Black bars indicate putatively functional genes and grey bars indicate pseudogenes. Pouched rats, rats, mice, squirrels, dogs, cattle, and pigs have similar numbers of reported olfactory receptor genes. Squirrels have a large number of pseudogenes.

Fig 4. Comparative gene tree of olfactory receptor sequences for pouched rat, mouse, rat, and squirrel.

Expansions are indicated with group identifiers and arrows. The tree is rooted at the branch separating Class I and Class II receptor clades. The Class I receptor clade is indicated with an open box.

Fig 5. Examples of orthologous olfactory receptor (OR) gene sequence among rodents.

Numbers at branch points indicate bootstrap values. A) 1-to-1 orthology between pouched rat, mouse, rat, and squirrel (Ictidomys tridecemilineatus) B) Example of pouched rat paralog within orthologous gene grouping.

Fig 6. Venn diagram of relative proportions of one-to-one orthology of pouched rat olfactory receptor genes and squirrel, mouse, and rat.

Pouched rats have the largest number of orthologous genes shared with mice and rats. The number of orthologous groupings with squirrels are consistently smaller than orthologies with mice or rats, due to phylogenetic placement.