Evolutionary origins of ultrasonic hearing and laryngeal echolocation in bats inferred from morphological analyses of the inner ear

PMCID: PMC3598973This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited

A phylogenomic analysis of the role and timing of molecular adaptation in the aquatic transition of cetartiodactyl mammals

This work was funded by the European Research Council (ERC 1076 Starting grant no. 310482) awarded to S.J.R. and a Newton International Fellowship awarded to M.R.M

The Evolution of Bat Vestibular Systems in the Face of Potential Antagonistic Selection Pressures for Flight and Echolocation

PMCID: PMC3634842This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Genome-wide signatures of convergent evolution in echolocating mammals

Evolution is typically thought to proceed through divergence of genes, proteins, and ultimately phenotypes(1-3). However, similar traits might also evolve convergently in unrelated taxa due to similar selection pressures(4,5). Adaptive phenotypic convergence is widespread in nature, and recent results from a handful of genes have suggested that this phenomenon is powerful enough to also drive recurrent evolution at the sequence level(6-9). Where homoplasious substitutions do occur these have long been considered the result of neutral processes. However, recent studies have demonstrated that adaptive convergent sequence evolution can be detected in vertebrates using statistical methods that model parallel evolution(9,10) although the extent to which sequence convergence between genera occurs across genomes is unknown. Here we analyse genomic sequence data in mammals that have independently evolved echolocation and show for the first time that convergence is not a rare process restricted to a handful of loci but is instead widespread, continuously distributed and commonly driven by natural selection acting on a small number of sites per locus. Systematic analyses of convergent sequence evolution in 805,053 amino acids within 2,326 orthologous coding gene sequences compared across 22 mammals (including four new bat genomes) revealed signatures consistent with convergence in nearly 200 loci. Strong and significant support for convergence among bats and the dolphin was seen in numerous genes linked to hearing or deafness, consistent with an involvement in echolocation. Surprisingly we also found convergence in many genes linked to vision: the convergent signal of many sensory genes was robustly correlated with the strength of natural selection. This first attempt to detect genome-wide convergent sequence evolution across divergent taxa reveals the phenomenon to be much more pervasive than previously recognised

Functional correlates of skull shape in Chiroptera: feeding and echolocation adaptations.

Morphological, functional and behavioural adaptations of bats are among the most diverse within mammals. A strong association between bat skull morphology and feeding behaviour has been suggested previously. However, morphological variation related to other drivers of adaptation, in particular echolocation, remains understudied. We assessed variation in skull morphology with respect to ecology (diet and emission type) and function (bite force, masticatory muscles and echolocation characteristics) using geometric morphometrics and comparative methods. Our study suggests that variation in skull shape of 10 bat families is the result of adaptations to broad dietary categories and sound emission types (oral or nasal). Skull shape correlates with echolocation parameters only in a subsample of insectivorous species, possibly because they (almost) entirely rely on this sensory system for locating and capturing prey. Insectivores emitting low frequencies are characterised by a ventrally tilted rostrum, a trait not associated with feeding parameters. This result questions the validity of a trade-off between feeding and echolocation function. Our study advances understanding of the relationship between skull morphology and specific features of echolocation and suggests that evolutionary constraints due to echolocation may differ between different groups within the Chiroptera

Functional Implications of Ubiquitous Semicircular Canal Non-Orthogonality in Mammals

The ‘canonical model’ of semicircular canal orientation in mammals assumes that 1) the three ipsilateral canals of an inner ear exist in orthogonal planes (i.e., orthogonality), 2) corresponding left and right canal pairs have equivalent angles (i.e., angle symmetry), and 3) contralateral synergistic canals occupy parallel planes (i.e., coplanarity). However, descriptions of vestibular anatomy that quantify semicircular canal orientation in single species often diverge substantially from this model. Data for primates further suggest that semicircular canal orthogonality varies predictably with the angular head velocities encountered in locomotion. These observations raise the possibility that orthogonality, symmetry, and coplanarity are misleading descriptors of semicircular canal orientation in mammals, and that deviations from these norms could have significant functional consequences. Here we critically assess the canonical model of semicircular canal orientation using high-resolution X-ray computed tomography scans of 39 mammal species. We find that substantial deviations from orthogonality, angle symmetry, and coplanarity are the rule for the mammals in our comparative sample. Furthermore, the degree to which the semicircular canals of a given species deviate from orthogonality is negatively correlated with estimated vestibular sensitivity. We conclude that the available comparative morphometric data do not support the canonical model and that its overemphasis as a heuristic generalization obscures a large amount of functionally relevant variation in semicircular canal orientation between species.Funding for this research was provided by grants NSFIIS-0208675 (http://www.nsf.gov/cise/iis/hcc_pgm.jsp), and EAR-0948842 (http://www.nsf.gov/awards/award_visualiz​ation.jsp?org=EAR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Geological SciencesAnthropologyEmail: [email protected]

A coalescent-based estimator of genetic drift, and acoustic divergence in the Pteronotus parnellii species complex

Dávalos, Liliana M., Lancaster, Winston C., Núñez-Novas, Miguel S., León, Yolanda M., Lei, Bonnie, Flanders, Jon, Russell, Amy L. (2018): A coalescent-based estimator of genetic drift, and acoustic divergence in the Pteronotus parnellii species complex. Heredity 122 (4): 417-427, DOI: 10.1038/s41437-018-0129-3, URL: http://dx.doi.org/10.1038/s41437-018-0129-

Limited Evidence for Parallel Molecular Adaptations Associated with the Subterranean Niche in Mammals: A Comparative Study of Three Superorders

Among mammals, several lineages have independently adapted to a subterranean niche and possess similar phenotypic traits for burrowing (e.g., cylindrical bodies, short limbs, and absent pinnae). Previous research on mole-rats has revealed molecular adaptations for coping with reduced oxygen, elevated carbon dioxide, and the absence of light. In contrast, almost nothing is known regarding molecular adaptations in other subterranean lineages (e.g., true moles and golden moles). Therefore, the extent to which the recurrent phenotypic adaptations of divergent subterranean taxa have arisen via parallel routes of molecular evolution remains untested. To address these issues, we analyzed 8,000 loci in 15 representative subterranean taxa of four independent transitions to an underground niche for signatures of positive selection and convergent amino acid substitutions. Complementary analyses were performed in nonsubterranean “control” taxa to assess the biological significance of results. We found comparable numbers of positively selected genes in each of the four subterranean groups; however, correspondence in terms of gene identity between gene sets was low. Furthermore, we did not detect evidence of more convergent amino acids among subterranean species pairs compared with levels found between nonsubterranean controls. Comparisons with nonsubterranean taxa also revealed loci either under positive selection or with convergent substitutions, with similar functional enrichment (e.g., cell adhesion, immune response, and coagulation). Given the limited indication that positive selection and convergence occurred in the same loci, we conclude that selectionmay have acted on different loci across subterraneanmammal lineages to produce similar phenotypes.The European Research Council (ERC Starting Grant 310482 [EVOGENO]) awarded to S.J.R. with additional support from the DST-NRF SARChI Chair for Behavioural Ecology and Physiology (Grant No. 64756) awarded to N.C.B. This research utilized Queen Mary’s Apocrita HPC Facility, supported by QMUL Research-IT (http://doi.org/10.5281/zenodo.438045).http://mbe.oxfordjournals.orgam2019Mammal Research InstituteZoology and Entomolog