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With diverse mechanical and sensory functions, the vertebrate cranium is a complex anatomical structure whose shifts between modularity and integration, especially in mechanical func- tion, have been implicated in adaptive diversification. Yet how me- chanical and sensory systems and their functions coevolve, as well as how their interrelationship contributes to phenotypic disparity, remain largely unexplored. To examine the modularity, integration, and evolutionary rates of sensory and mechanical structures within the head, we analyzed hard and soft tissue scans from ecologically diverse bats in the superfamily Noctilionoidea, a clade that ranges from insectivores and carnivores to frugivores and nectarivores. We identified eight regions that evolved in a coordinated fashion, thus recognizable as evolutionary modules: five associated with bite force and three linked to olfactory, visual, and auditory systems. Interrelationships among these modules differ between Neotropical leaf-nosed bats (family Phyllostomidae) and other noctilionoids. Consistent with the hypothesis that dietary transitions begin with changes in the capacity to detect novel food items followed by adap- tations to process them, peak rates of sensory module evolution pre- date those of some mechanical modules. We propose that the co- evolution of structures influencing bite force, olfaction, vision, and hearing constituted a structural opportunity that allowed the phyllostomid ancestor to take advantage of existing ecological op- portunities and contributed to the clade’s remarkable radiation. 

It has been recognized as early as the Victorian era that the apex of the distal phalanx has a distinct embryological development from the main shaft of the distal phalanx. Recent studies in regenerative medicine have placed an emphasis on the role of the apex of the distal phalanx in bone regrowth. Despite knowledge about the unique aspects of the distal phalanx, all phalanges are often treated as equivalent. Our morphological study reiterates and highlights the special anatomical and embryological properties of the apex of the distal phalanx, and names the apex “the bony cap” to distinguish it. We posit that the distal phalanx shaft is endochondral, while the bony cap is intramembranous and derived from the ectodermal wall. During development, the bony cap may be a separate structure that will fuse to the endochondral distal phalanx in the adult, as it ossifies well before the distal phalanges across taxa. Our study describes and revives the identity of the bony cap, and we identify it in three mammalian species: humans, cats, and horses ( Homo sapiens, Felis catus domestica , and Equus caballus ). During the embryonic period, we show the bony cap has a thimble-like shape that surrounds the proximal endochondral distal phalanx. The bony cap may thus play an inductive role in the differentiation of the corresponding nail, claw, or hoof (keratin structures) of the digit. When it is not present or develops erroneously, the corresponding keratin structures are affected, and regeneration is inhibited. By terming the bony cap, we hope to inspire more attention to its distinct identity and role in regeneration. 

The extensive diversity observed in bat nasal chemosensory systems has been well‐documented at the histological level. Understanding how this diversity evolved and developing hypotheses as to why particular patterns exist require a phylogenetic perspective, which was first outlined in the work of anatomist Kunwar Bhatnagar. With the onset of genetics and genomics, it might be assumed that the puzzling patterns observed in the morphological data have been clarified. However, there is still a widespread mismatch of genetic and morphological correlations among bat chemosensory systems. Novel genomic evidence has set up new avenues to explore that demand more evidence from anatomical structures. Here, we outline the progress that has been made in both morphological and molecular studies on the olfactory and vomeronasal systems in bats since the work of Bhatnagar. Genomic data of olfactory and vomeronasal receptors demonstrate the strong need for further morphological sampling, with a particular focus on receiving brain regions, glands, and ducts.

 

Following the draft sequence of the first human genome over 20 years ago, we have achieved unprecedented insights into the rules governing its evolution, often with direct translational relevance to specific diseases. However, staggering sequence complexity has also challenged the development of a more comprehensive understanding of human genome biology. In this context, interspecific genomic studies between humans and other animals have played a critical role in our efforts to decode human gene families. In this review, we focus on how the rapid surge of genome sequencing of both model and non-model organisms now provides a broader comparative framework poised to empower novel discoveries. We begin with a general overview of how comparative approaches are essential for understanding gene family evolution in the human genome, followed by a discussion of analyses of gene expression. We show how homology can provide insights into the genes and gene families associated with immune response, cancer biology, vision, chemosensation, and metabolism, by revealing similarity in processes among distant species. We then explain methodological tools that provide critical advances and show the limitations of common approaches. We conclude with a discussion of how these investigations position us to gain fundamental insights into the evolution of gene families among living organisms in general. We hope that our review catalyzes additional excitement and research on the emerging field of comparative genomics, while aiding the placement of the human genome into its existentially evolutionary context.

 

Abstract Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants. 

Abstract Evolution has shaped the limbs of hoofed animals in specific ways. In artiodactyls, it is the common assumption that the metatarsal is composed of the fusion of digits III and IV, whereas the other three digits have been lost or are highly reduced. However, evidence from the fossil record and internal morphology of the metatarsal challenges these assumptions. Furthermore, only a few taxonomic groups have been analysed. In giraffes, we discovered that all five digits are present in the adult metatarsal and are highly fused and modified rather than lost. We examined high-resolution micro-computed tomography scans of the metatarsals of two mid and late Miocene giraffid fossils and the extant giraffe and okapi. In all the Giraffidae analysed, we found a combination of four morphologies: (1) four articular facets; (2) four or, in most cases, five separate medullary cavities internally; (3) a clear, small digit I; and (4) in the two fossil taxa of unknown genus, the presence of external elongated grooves where the fusions of digits II and V have taken place. Giraffa and Okapia, the extant Giraffidae, show a difference from all the extinct taxa in having more flattened digits tightly packed together, suggesting convergent highly fused digits despite divergent ecologies and locomotion. These discoveries provide evidence that enhances our understanding of how bones fuse and call into question current hypotheses of digit loss. 

While evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness-related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant-visiting from an insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant-visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant-visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants — a potential ecological constraint on sensory evolution. 

Abstract Chemosensation is the most ubiquitous sense in animals, enacted by the products of complex gene families that detect environmental chemical cues and larger-scale sensory structures that process these cues. While there is a general conception that olfactory receptor (OR) genes evolve rapidly, the universality of this phenomenon across vertebrates, and its magnitude, are unclear. The supposed correlation between molecular rates of chemosensory evolution and phenotypic diversity of chemosensory systems is largely untested. We combine comparative genomics and sensory morphology to test whether OR genes and olfactory phenotypic traits evolve at faster rates than other genes or traits. Using published genomes, we identified ORs in 21 tetrapods, including amphibians, reptiles, birds, and mammals and compared their rates of evolution to those of orthologous non-OR protein-coding genes. We found that, for all clades investigated, most OR genes evolve nearly an order of magnitude faster than other protein-coding genes, with many OR genes showing signatures of diversifying selection across nearly all taxa in this study. This rapid rate of evolution suggests that chemoreceptor genes are in “evolutionary overdrive,” perhaps evolving in response to the ever-changing chemical space of the environment. To obtain complementary morphological data, we stained whole fixed specimens with iodine, µCT-scanned the specimens, and digitally segmented chemosensory and nonchemosensory brain regions. We then estimated phenotypic variation within traits and among tetrapods. While we found considerable variation in chemosensory structures, they were no more diverse than nonchemosensory regions. We suggest chemoreceptor genes evolve quickly in reflection of an ever-changing chemical space, whereas chemosensory phenotypes and processing regions are more conserved because they use a standardized or constrained architecture to receive and process a range of chemical cues. 

Abstract Dietary adaptation is a major feature of phenotypic and ecological diversification, yet the genetic basis of dietary shifts is poorly understood. Among mammals, Neotropical leaf-nosed bats (family Phyllostomidae) show unmatched diversity in diet; from a putative insectivorous ancestor, phyllostomids have radiated to specialize on diverse food sources including blood, nectar, and fruit. To assess whether dietary diversification in this group was accompanied by molecular adaptations for changing metabolic demands, we sequenced 89 transcriptomes across 58 species and combined these with published data to compare ∼13,000 protein coding genes across 66 species. We tested for positive selection on focal lineages, including those inferred to have undergone dietary shifts. Unexpectedly, we found a broad signature of positive selection in the ancestral phyllostomid branch, spanning genes implicated in the metabolism of all major macronutrients, yet few positively selected genes at the inferred switch to plantivory. Branches corresponding to blood- and nectar-based diets showed selection in loci underpinning nitrogenous waste excretion and glycolysis, respectively. Intriguingly, patterns of selection in metabolism genes were mirrored by those in loci implicated in craniofacial remodeling, a trait previously linked to phyllostomid dietary specialization. Finally, we show that the null model of the widely-used branch-site test is likely to be misspecified, with the implication that the test is too conservative and probably under-reports true cases of positive selection. Our findings point to a complex picture of adaptive radiation, in which the evolution of new dietary specializations has been facilitated by early adaptations combined with the generation of new genetic variation.