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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.

 

Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size ( i.e. , body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels. 

Bite force is a performance metric commonly used to link cranial morphology with dietary ecology, as the strength of forces produced by the feeding apparatus largely constrains the foods an individual can consume. At a macroevolutionary scale, there is evidence that evolutionary changes in the anatomical elements involved in producing bite force have contributed to dietary diversification in mammals. Much less is known about how these elements change over postnatal ontogeny. Mammalian diets drastically shift over ontogeny—from drinking mother's milk to feeding on adult foods—presumably with equally drastic changes in the morphology of the feeding apparatus and bite performance. Here, we investigate ontogenetic morphological changes in the insectivorous big brown bat (Eptesicus fuscus), which has an extreme, positive allometric increase in bite force during development. Using contrast‐enhanced micro‐computed tomography scans of a developmental series from birth to adult morphology, we quantified skull shape and measured skeletal and muscular parameters directly related to bite force production. We found pronounced changes in the skull over ontogeny, including a large increase in the volume of the temporalis and masseter muscles, and an expansion of the skull dome and sagittal crest that would serve to increase the temporalis attachment area. These changes indicate that development of the jaw adductors play an important role in the development of biting performance of these bats. Notably, static bite force increases with positive allometry with respect to all anatomical measures examined, suggesting that modifications in biting dynamics and/or improved motor coordination also contribute to increases in biting performance.

 

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.

 

Traits for prey acquisition form the phenotypic interface of predator–prey interactions. In venomous predators, morphological variation in venom delivery apparatus like fangs and stingers may be optimized for dispatching prey. Here, we determine how a single dimension of venom injection systems evolves in response to variation in the size, climatic conditions and dietary ecology of viperid snakes. We measured fang length in more than 1900 museum specimens representing 199 viper species (55% of recognized species). We find both phylogenetic signal and within-clade variation in relative fang length across vipers suggesting both general taxonomic trends and potential adaptive divergence in fang length. We recover positive evolutionary allometry and little static allometry in fang length. Proportionally longer fangs have evolved in larger species, which may facilitate venom injection in more voluminous prey. Finally, we leverage climatic and diet data to assess the global correlates of fang length. We find that models of fang length evolution are improved through the inclusion of both temperature and diet, particularly the extent to which diets are mammal-heavy diets. These findings demonstrate how adaptive variation can emerge among components of complex prey capture systems. 

Dedicated nectarivory is a derived feeding habit that requires specialized cranial and soft‐tissue morphologies to extract nectar from flowers. Nectarivory has evolved many times in terrestrial vertebrates, and in four bat families (Pteropodidae, Phyllostomidae, Vespertilionidae, and Mystacinidae). Within phyllostomids, specializations to nectarivory have been well documented in two subfamilies, Glossophaginae and Lonchophyllinae. However, nectarivory has also evolved independently in the genusPhyllostomus(subfamily Phyllostominae). SincePhyllostomusspecies have an omnivorous diet with a high consumption of nectar, they can be used to explore the basic morphological modifications linked to evolving a nectarivorous habit. Here, we focused on describing and comparing the morphological features potentially associated with nectarivory inPhyllostomus discolor. We present the first detailed tongue and palate morphological descriptions forP. discolorand perform skull morphometric analysis including 10 species. We found hair‐like papillae on the tongue ofP. discolor, a convergent feature with Glossophaginae and nectarivorous Pteropodids; these papillae likely confer an advantage when feeding on nectar.P. discolordoes not show skull morphological features characteristic of nectarivorous bats, such as a long and narrow snout. We pose that the consumption of a variety of food, such as hard insects and fruits, and the large size ofP. discolorrelative to specialized nectarivores may create trade‐offs against morphological specialization of the skull towards nectarivory. In contrast, a long and mobile tongue with hair‐like papillae may be an evolutionary solution for nectar extraction that does not have a major impact on this species' ability to feed on other resources.

 

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.