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Dissecting the genetic basis of divergent and convergent evolution: From individuals to species radiations

Final Report Summary - EVOGENO (Dissecting the genetic basis of divergent and convergent evolution: From individuals to species radiations)

EVOGENO aimed to determine the genetic basis of evolutionary adaptations among mammals, particularly with respect to shifts to new physical, ecological and sensory niches. We were particularly concerned with whether unrelated mammal groups that have undergone shifts to the same niche have experienced selection at the same genes and gene pathways (so-called molecular convergence). The alternative scenario, more commonly accepted, is that molecular changes underpinning adaptation proceed via divergent evolutionary trajectories. To tackle our overarching aims we focused on several groups and systems that show forms of parallel phenotypic evolution over different phylogenetic timescales: among superorders, among orders within a superorder, among families within an order, and among species within a family. For each of these parts we built very large sequence datasets comprising thousands of genes and tens of taxa; these were generated from our own genomic and transcriptomic datasets based on high quality genetic material collected in the project, which we supplemented with published genomic sequences. We processed these data by developing bioinformatics pipelines to conduct genome-wide scans for accelerated substitutions, molecular adaptation and convergence.

First, to test for parallelism involved in shifts to new habitats, we compared highly divergent lineages of subterranean mammal from three different superorders, which show similar body forms and have independently transitioned to a niche below ground. Our genome-wide studies of molecular adaptation relating to the subterranean niche in mammals point to broadly divergent routes of molecular adaptation, in which selection acted on different loci to produce similar phenotypes. Within a superorder, we tested for genetic convergence related to sensory perception between echolocating bats and cetaceans, which both show shifts to reliance on audition and away from vision. Our findings revealed new evidence of parallel amino acid substitutions in loci that have not previously been studied in this context. Also in echolocating cetaceans, we found strong evidence for stepwise molecular adaptation, involving numerous loci, leading to extreme high frequency hearing in dolphins, and we also generated the first fully-resolved phylogenetic tree of cetaceans.

At shallower timeframes, we focused on bats, specifically comparing lineages from distant suborders that have both evolved constant frequency echolocation. We discovered limited convergence associated with the evolution of this form of echolocation in neotropical and Old World bats, and also found that the evolution of this trait in neotropical bats was a multistep process over evolutionary time. We also examined the single family Phyllostomidae, a neotropical radiation in which members show diversification in diet and associated divergence and convergent in sensory modalities. Our data revealed parallel losses of shortwave vision in related bat species have proceeded through divergent genetic routes involving interruptions in transcription and translation. Also in these bats, we discovered that the evolution of different sensory modalities and diets has involved molecular adaptation in genes involved in lens development, as well as selection in different sets of metabolism genes. Most notably, these analyses have revealed strong evidence of divergent trajectories linked to evolutionary switches in diet, with insect-eating bats showing more molecular adaptation in loci involved in protein metabolism, and fruit- and nectar feeding bats showing selection and remarkable convergence in genes that function in carbohydrate metabolism. Finally, we used our sets of candidate echolocation genes to test whether the same loci have been targets of selection among newly diverging species, looking at horseshoe bats specifically. Our results from this study revealed that divergence incipient species is associated with islands of divergence in, or adjacent to, genes implicated in hearing as well as in body size variation.