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Report

Teaser, summary, work performed and final results

Periodic Reporting for period 2 - ConvergeAnt (An Integrative Approach to Understanding Convergent Evolution in Ant-eating Mammals)

Teaser

Summary

Understanding how different species repeatedly adapted to similar environmental constraints is one of the fundamental topics in evolutionary biology. Despite its widespread occurrence at many levels across the tree of life, fundamental questions still remain unanswered concerning the fascinating phenomenon of convergent evolution. By providing natural evolutionary replay experiments, convergently evolved taxa have the potential to shed light on the predictability of evolution. The convergent evolution of species living in similar environments illustrates the power of natural selection to produce phenotypic similarity despite different evolutionary histories. The large extent of convergent morphological evolution, the importance of molecular convergence, and the potential role of the host microbiome are gaining acceptance. The ConvergeAnt project aimed at tackling these questions by studying ant-eating mammals, which constitute a textbook example of morphological convergence with at least five independent origins in placentals (armadillos, anteaters, aardvarks, pangolins, and aardwolves). Taking advantage of the unique set of convergently evolved characters associated with the ant-eating diet, we investigate the molecular mechanisms underlying phenotypical adaptation through an integrative approach combining morphometric, genomic, and metagenomic approaches. The ultimate objective of the ConvergeAnt project is to provide fundamental insights into the complex interplay between the morphology, the genome, and the microbiome in a classical case of adaptive convergence driven by a highly specialized diet.

Work performed

This first half of the project has focused on the morphological and genomic aspects of the project. For these two tasks, we have delivered a wealth of data that have been key to the project. For the morphological task, 3D digital data from skulls have been collected via X-ray micro-computed tomography (Î¼CT) and MicroScribe 3D digitizer for a total of more than 100 and 700 specimens, respectively. New Î¼CT-scan data have been used to characterize the evolutionary processes by which convergent dental reduction occurs. We showed that convergent tooth loss in anteaters and pangolins resulted in a different fate of the mandibular canal with anteaters still presenting tooth neurovascular systems (dorsal canaliculi) in their mandible while pangolins do not. As in baleen whales, osseous and neurovascular structures of the anteater mandible were rewired following the loss of teeth probably to sustain a sensory function. This implies that the external resemblances of the mandibles in anteaters and pangolins have overshadowed the complex evolution of their internal morphology. For the genomic task, we unlocked a major challenge by showing that a hybrid sequencing strategy could be successfully used to produce high-quality genomes for roadkill leading to the production of seven complete genomes of elusive myrmecophagous species that will be used to unravel the genomic mechanisms underlying convergent ant-eating phenotypes. A major result for this task concerns the evolution of chitinase genes (CHIAs), which encode enzymes capable of digesting insect exoskeletal chitin. By conducting a detailed genomic survey of those genes, we were able to infer that the ancestor of all placental mammals likely possessed five functional CHIA genes, a results that fits perfectly with its insectivorous diet inferred from the fossil record. Many CHIA functional copies were rapidly pseudogenized as placentals radiated into different dietary niches following the demise of non-avian dinosaurs with the number of functional CHIAs positively correlating with the percentage of invertebrates in the diet. Our results demonstrate that placental mammal genomes retained a molecular record of placental adaptive radiation in the form of numerous chitinase pseudogenes with again different evolutionary fates among myrmecophagous species. Indeed anteaters, armadillos, and aardvarks retaining 4-5 functional CHIA copies whereas pangolins and aardwolves only have one. This suggests that these convergent species used different mechanisms to digest ants and termites possibly through differences in gene expression and/or gut microbiomes.

Final results

At project mid-term, we start understanding how convergent lineages of ant-eating mammals have evolved. Our results already revealed that convergent evolution proceeded through different underlying mechanisms in anteaters and pangolins at both the phenotypic level with the example of the mandibular canal, but also at the genomic level with the discovery of different chitinase genes involved in social insect digestion in these two ancient ant-eating lineages. The new phenotypic and genomic data gathered so far will allow digging deeper into the mechanisms involved in convergent evolution. On the morphological front, we are currently using the Î¼CT-scan data to explore the evolution of neglected features of the skull such as turbinal bones, nasal sinuses, and the cribriform plate in order to understand how these structures have coevolved in convergent ant-eating lineages. The 3D-digitized specimens will also be used for testing levels of skull shape integration in convergent lineages with modularity methods. Furthermore, detailed digital dissections of masticatory muscles will allow finely characterizing the processes associated with tooth reduction/loss and muzzle elongation in the different ant-eating lineages. On the genomic front, the high-quality genomes produced for seven ant-eating species will be explored to unravel the genomic mechanisms underlying the previously characterized convergent ant-eating phenotypes. The high quality of our genomes in terms of both contiguity and completeness will permit applying state of the art statistical methods for detecting convergent molecular evolution on both protein-coding and non-coding regions, but also to confidently assess patterns of gene loss and pseudogenization. Additionally, the transcriptomes obtained from salivary glands will allow quantifying the expression of specific genes such as digestives enzymes in convergent ant-eating lineages. Finally, on the microbiome front, we will first use the hundreds of already collected samples to assess the diversity and the patterns of phylosymbiosis of gut microbes in ant-eating lineages and closely related species. Complementarily, shotgun metagenomic analyses will be conducted to characterize the microbial functional diversity in convergent ant-eating species in order to precise the potential role played by the microbiome in the convergent adaptation to this highly specialized diet. Combining these three approaches will significantly improved our understanding of the mechanisms underlying this textbook example of convergent evolution.