Adaptations and convergences of the olfactory system in small insectivorous placental mammals – RHINOGRAD

Understanding how species adapted to their environment has been one of the most intensively studied fields in evolutionary biology. The most spectacular shifts in morphology and ecology seem to be the result of historical events, such as mass extinctions or island formation. Such events provide new ecological opportunities to survivors or dispersers and create the conditions for adaptive radiations Within highly diversified lineages, evolutionary convergence often is (1) a prominent feature of adaptive radiation, (2) generates high morphological diversity within replicated environment, and (3) provides compelling evidence supporting natural selection as a primary mechanism of diversification. Recent advances in X-ray microtomography (X-ray µCT), functional anatomy, and genomics give us the opportunity to study the different aspects of how organisms adapt and converge to their environment. This project proposes a novel “pheno-genomic” approach to studying olfactory adaptations and convergences in small insectivorous placental mammals.
The repeated evolution of insectivorous adaptation in placentals provides classical cases of morphological adaptation and convergence. Insectivorous diet was usually seen as a plesiomorphic diet in mammals. However, several natural and independent experiments have occurred in placentals, making them an ideal biological system to study both adaptations and convergences. Hunting highly mobile preys within terrestrial, underground or aquatic habitats has put them under adaptive pressure in terms of olfactory and thermic-loss constraints. Until recently, descriptions of the rostrum relied on the sectioning of heads or skulls, making it difficult to visualize them in three dimensions and limiting the number of species that could be studied due to the destructive nature of the methods. However, advances in non-destructive imaging technology have made it possible to visualize the inner turbinates and associated cranial sinuses in silico and opened the door for broader comparative studies of their structure and function. Here, we propose to use turbinate surface area as a proxy for olfactory epithelial surface area and to compare this parameter across a large sample of insectivorous small mammals including Eulipotyphla, Scandentia, Rodentia, and Afrosoricida. By doing so, we will test whether olfactory surface area is negatively correlated with degree of insectivorous diet, and lifestyle. Secondly, genes underlying key phenotypic adaptations can now be targeted and analyzed for evidence of natural selection, a valuable strategy that has yet to be unified with morphological data. We propose to develop a “pheno-genomic” approach to study adaptation by focusing on the genetics of olfaction, which is expected to have evolved in the context of insectivory in mammals. We will combine targeted resequencing on gene families involved in olfaction (olfactory receptors ORs and vomeronasal receptors VRs), and RNA sequencing on tissues where these genes are expressed to quantify variation in sequence, expression and gene repertoire of these candidate genes between sets of independently evolved insectivorous and non-insectivorous lineages. Signatures of genes under positive selection and pseudogene quantification will provide a mechanistic basis for evaluating the environmental drivers of turbinate surface and testing hypotheses about rostrum adaptation. Using an integrative approach linking morphology, genomics, and comparative methods, our objective is to address the following questions on deterministic evolutionary mechanisms: do transitions toward different insectivorous diet and lifestyles involved adaptations of their olfactory systems among convergent lineages? What are the consequences of these olfactory adaptations on their morphologies, performances, and genomes? What are the directions and strength of pheno-genomic convergences among insectivorous lineages?