Abstract
The speciose mammalian order Eulipotyphla (moles, shrews, hedgehogs, solenodons) combines an unusual diversity of semi-aquatic, semi-fossorial, and fossorial forms that arose from terrestrial forbearers. However, our understanding of the ecomorphological pathways leading to these lifestyles has been confounded by a fragmentary fossil record, unresolved phylogenetic relationships, and potential morphological convergence, calling for novel approaches. The net surface charge of the oxygen-storing muscle protein myoglobin (ZMb), which can be readily determined from its primary structure, provides an objective target to address this question due to mechanistic linkages with myoglobin concentration. Here, we generate a comprehensive 71 species molecular phylogeny that resolves previously intractable intra-family relationships and then ancestrally reconstruct ZMb evolution to identify ancient lifestyle transitions based on protein sequence alone. Our phylogenetically informed analyses confidently resolve fossorial habits having evolved twice in talpid moles and reveal five independent secondary aquatic transitions in the order housing the world's smallest endothermic divers.
Highlights
A fundamental challenge of evolutionary biology is to understand the phylogenomic foundations of biochemical and physiological specializations that have enabled organisms to proliferate into new adaptive zones
Consistent with previous surveys that indicate that myoglobin occurs as a single-copy, 210 orthologous gene in the genomes of mammals and other jawed vertebrates (Schwarze et al, 2014), with rare, lineage-specific gene duplications being restricted to certain aquatic lineages such as some Cyprininae and Dipnoi, we found no evidence for gene paralogues in any of the species 214 examined, with conceptual translations revealing the expected 153 amino-acid peptides in most cases
The phylogenetic estimates constructed from our comprehensive tree-of-life gene set provide a robust framework to interpret ecomorphological evolution within Eulipotyphla
Summary
A fundamental challenge of evolutionary biology is to understand the phylogenomic foundations of biochemical and physiological specializations that have enabled organisms to proliferate into new adaptive zones. Mirceta et al (2013) extended this work to reveal that maximal muscle myoglobin concentration was mechanistically linked to myoglobin net surface charge (ZMb) in mammals via adaptive changes in primary structure, with convergent increases in ZMb found in members of all eight lineages with an extended aquatic/semi-aquatic evolutionary history This trait presumably represents an adaptive response to combat the general propensity for proteins to precipitate at high concentration, thereby allowing for advantageous elevations of this muscle O2 store without deleterious self-aggregation (Mirceta, et al 2013). Current phylogenetic hypotheses for Eulipotyphla lack definitive resolution below the family level (He, et al 2010; He, et al 2017) thereby precluding reliable ancestral reconstructions To overcome these shortcomings, we used a capture hybridization approach to target coding sequences of myoglobin together with 25 tree-of-life genes from 61 eulipotyphlan DNA libraries (44 moles, 11 shrews, 5 hedgehogs, and 1 solenodon) that included representatives from all seven recognized semi-aquatic genera within this order. Having shown that these important conditions are met, we traced ZMb across eulipotyphlan evolutionary history, thereby allowing us to determine when and how many times semi-aquatic specializations for increased dive durations evolved in both shrews and moles, and evaluate alternative evolutionary scenarios of talpid lifestyle evolution
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