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Abstract Neotropical leaf-nosed bats (family Phyllostomidae) underwent an impressive adaptive radiation characterized primarily by the diversification of dietary strategies in tandem with functional morphological diversification of their craniodental and sensory systems. In this perspective, we integrate information from extensive research across multiple fields to outline the interplay between extrinsic and intrinsic drivers of the phyllostomid adaptive radiation and the resulting ecomorphological diversity of the clade. We begin by exploring the relationship between phyllostomids and their environments, focusing on the ecogeographical drivers of their radiation. Then, we detail current knowledge about the role of genes and development in enabling morphological diversification of the group. Finally, we describe the breathtaking ecomorphological diversification of phyllostomids, trying to unveil functional connections underlying their diverse dietary niches. 

Adaptive radiations are bursts in biodiversity that generate new evolutionary lineages and phenotypes. However, because they typically occur over millions of years, it is unclear how their macroevolutionary dynamics vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets-from insects to vertebrates, fruit, nectar, and blood-and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; phyllostomids' initial, higher-level diversification involved an "early burst" in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified within broad adaptive zones, likely reflecting finer-scale niche partitioning. Importantly, the observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the value of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic levels, with early bursts being more common at higher levels. 

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. 

Abstract BackgroundThrough the evolution of novel wing structures, bats (Order Chiroptera) became the only mammalian group to achieve powered flight. This achievement preceded the massive adaptive radiation of bats into diverse ecological niches. We investigate some of the developmental processes that underlie the origin and subsequent diversification of one of the novel membranes of the bat wing: the plagiopatagium, which connects the fore- and hind limb in all bat species. ResultsOur results suggest that the plagiopatagium initially arises through novel outgrowths from the body flank that subsequently merge with the limbs to generate the wing airfoil. Our findings further suggest that this merging process, which is highly conserved across bats, occurs through modulation of the programs controlling the development of the periderm of the epidermal epithelium. Finally, our results suggest that the shape of the plagiopatagium begins to diversify in bats only after this merging has occurred. ConclusionsThis study demonstrates how focusing on the evolution of cellular processes can inform an understanding of the developmental factors shaping the evolution of novel, highly adaptive structures. 

Abstract Tooth classes are an innovation that has contributed to the evolutionary success of mammals. However, our understanding of the mechanisms by which tooth classes diversified remain limited. We use the evolutionary radiation of noctilionoid bats to show how the tooth developmental program evolved during the adaptation to new diet types. Combining morphological, developmental and mathematical modeling approaches, we demonstrate that tooth classes develop through independent developmental cascades that deviate from classical models. We show that the diversification of tooth number and size is driven by jaw growth rate modulation, explaining the rapid gain/loss of teeth in this clade. Finally, we mathematically model the successive appearance of tooth buds, supporting the hypothesis that growth acts as a key driver of the evolution of tooth number and size. Our work reveal how growth, by tinkering with reaction/diffusion processes, drives the diversification of tooth classes and other repeated structure during adaptive radiations. 

Abstract The evolution of complex dentitions in mammals was a major innovation that facilitated the expansion into new dietary niches, which imposed selection for tight form–function relationships. Teeth allow mammals to ingest and process food items by applying forces produced by a third-class lever system composed by the jaw adductors, the cranium, and the mandible. Physical laws determine changes in jaw adductor (biting) forces at different bite point locations along the mandible (outlever), thus, individual teeth are expected to experience different mechanical regimes during feeding. If the mammal dentition exhibits functional adaptations to mandible feeding biomechanics, then teeth are expected to have evolved to develop mechanically advantageous sizes, shapes, and positions. Here, we present bats as a model system to test this hypothesis and, more generally, for integrative studies of mammal dental diversity. We combine a field-collected dataset of bite forces along the tooth row with data on dental and mandible morphology across 30 bat species. We (1) describe, for the first time, bite force trends along the tooth row of bats; (2) use phylogenetic comparative methods to investigate relationships among bite force patterns, tooth, and mandible morphology; and (3) hypothesize how these biting mechanics patterns may relate to the developmental processes controlling tooth formation. We find that bite force variation along the tooth row is consistent with predictions from lever mechanics models, with most species having the greatest bite force at the first lower molar. The cross-sectional shape of the mandible body is strongly associated with the position of maximum bite force along the tooth row, likely reflecting mandibular adaptations to varying stress patterns among species. Further, dental dietary adaptations seem to be related to bite force variation along molariform teeth, with insectivorous species exhibiting greater bite force more anteriorly, narrower teeth and mandibles, and frugivores/omnivores showing greater bite force more posteriorly, wider teeth and mandibles. As these craniodental traits are linked through development, dietary specialization appears to have shaped intrinsic mechanisms controlling traits relevant to feeding performance. 

Synopsis Among the developmental processes that have been proposed to influence the direction of evolution, the modular organization of developmental gene regulatory networks (GRNs) has shown particular promise. In theory, GRNs have core modules comprised of essential, conserved circuits of genes, and sub-modules of downstream, secondary circuits of genes that are more susceptible to variation. While this idea has received considerable interest as of late, the field of evo-devo lacks the experimental systems needed to rigorously evaluate this hypothesis. Here, we introduce an experimental system, the vertebrate tooth, that has great potential as a model for testing this hypothesis. Tooth development and its associated GRN have been well studied and modeled in both model and non-model organisms. We propose that the existence of modules within the tooth GRN explains both the conservation of developmental mechanisms and the extraordinary diversity of teeth among vertebrates. Based on experimental data, we hypothesize that there is a conserved core module of genes that is absolutely necessary to ensure tooth or cusp initiation and development. In regard to tooth shape variation between species, we suggest that more relaxed sub-modules activated at later steps of tooth development, for example, during the morphogenesis of the tooth and its cusps, control the different axes of tooth morphological variation. 

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. 

The loss of previously adaptive traits is typically linked to relaxation in selection, yet the molecular steps leading to such repeated losses are rarely known. Molecular studies of loss have tended to focus on gene sequences alone, but overlooking other aspects of protein expression might underestimate phenotypic diversity. Insights based almost solely on opsin gene evolution, for instance, have made mammalian color vision a textbook example of phenotypic loss. We address this gap by investigating retention and loss of opsin genes, transcripts, and proteins across ecologically diverse noctilionoid bats. We find multiple, independent losses of short-wave-sensitive opsins. Mismatches between putatively functional DNA sequences, mRNA transcripts, and proteins implicate transcriptional and post-transcriptional processes in the ongoing loss of S-opsins in some noctilionoid bats. Our results provide a snapshot of evolution in progress during phenotypic trait loss, and suggest vertebrate visual phenotypes cannot always be predicted from genotypes alone.