Biology subjects

Santana, S. E.

Publications and source records attributed to Santana, S. E..

11 recordsLinked to original sources

bioRxiv2026

Functional tradeoffs promote morphological disparity in the bat nasal cavity

Multifunctional anatomical structures must accommodate potentially competing performance demands, leading to functional tradeoffs. The mammal rostrum (snout) is involved in multiple functions, including feeding, respiratory conditioning, olfaction, and, in most bats, echolocation. Therefore, it serves as an ideal system to investigate whether and how functional tradeoffs promote or constrain morphological diversification. While the external morphology of the rostrum has been linked with mechanical demands of feeding in bats, the factors and processes influencing its internal morphology, including the turbinals in the nasal cavity, remain comparatively unexplored. Here we investigate how internal rostral morphology reflects specialization and tradeoffs among respiratory air conditioning, echolocation, and olfaction by quantifying turbinal morphological diversity in a phylogenetically and ecologically diverse sample of bat species. We find that echolocation mode predominantly influences both the ethmoturbinal complex (ETc) and maxilloturbinal (MT) systems, with nasal-emitting bats having reduced and less complex turbinals compared to oral and non-laryngeally echolocating bat species. MT complexity and surface area are not associated with bioclimatic variables representing thermal variability and aridity. However, the ETc exhibits higher complexity in plantivorous bats than faunivorous bats, suggesting higher olfactory reliance. While MT morphological disparity was predominantly explained by echolocation mode, ETc morphological disparity was associated with both echolocation mode and diet, suggesting potentially opposing demands favoring turbinal reduction for sound transmission and elaboration for olfaction. Among nasal emitters, which must accommodate both demands within the nasal cavity, ETc complexity exhibited higher relative disparity compared to MT complexity. These patterns suggest that competing functional demands may promote or maintain morphological diversity, possibly through ecological specialization and/or many-to-one mapping between morphology and performance.

evolutionary biology↗

bioRxiv2026

Dietary specializations are captured by jaw muscle proportions in mammals

Mammalian diet and feeding ecology are often reflected by craniofacial skeleton specializations, but feeding requires skeletal actuation by a complex suite of muscles with varying sizes, lines of action, and mechanical function. While muscles play a critical role in feeding mechanics, and hence diet, it remains unclear how well variation in jaw muscle morphology predicts diet in mammals. We quantified the evolutionary interplay between mammalian muscle morphology and diet using a large and taxonomically broad sample. We measured the relative proportions and putative force production capacity, quantified as muscle physiological cross-sectional area (PCSA), for the major adductor complexes, along with a key jaw depressor, in 91 mammalian species (30 chiropterans, 33 primates, and 28 ungulates, carnivorans, rodents, and marsupials). We recovered clear dietary signals for several muscle complexes, with the medial pterygoid (larger in herbivores) and temporalis (larger in carnivores) performing best as dietary predictors. The medial pterygoid is particularly relevant for the mechanical innovation in mammals of moving the mandible along non-orthal, medio-lateral trajectories during mastication. Our findings underscore the intuitive, yet previously unquantified, importance of muscles in the evolution of mandibular roll, yaw, and lateral translation, all mammalian hallmarks of processing diverse types of food.

zoology↗

bioRxiv2024

Convergent mechanisms, divergent strategies: a comparison of nectar intake between a generalist and a specialized bat species

Nectar-feeding bats exhibit a range of specialized adaptations that allow them to efficiently extract nectar from flowers. These adaptations include diverse tongue morphological traits and feeding strategies that reflect varying degrees of specialization for nectarivory. While the feeding mechanisms of highly specialized nectar-feeding bats are well-studied, little is known about the feeding behaviors of non-specialized species like Phyllostomus discolor. This study compares the nectar extraction behaviors of P. discolor and the specialized Anoura geoffroyi, examining morphological and biomechanical adaptations that affect nectar-feeding efficiency and foraging strategies. Using high-speed videography, we analyzed the feeding behaviors of both species, focusing on tongue kinematics, and feeding efficiency. Both species used a brush-tongue lapping technique but exhibited notable behavioral and kinematic differences, resulting in efficiency variations. P. discolor has a shorter, less flexible tongue than A. geoffroyi, though its tongue shows similar mobility capacities (licking frequency). Unlike A. geoffroyi, which hovers to feed, P. discolor lands, allowing for longer visits and greater nectar extraction per visit. However, P. discolor demonstrated lower feeding efficiency, likely due to its reduced tongue specialization for nectarivory. These findings reveal convergence in the general feeding mechanism but highlight differences in morphological and behavioral specialization that affect feeding kinematics and efficiency. Our study illuminates how foraging strategy and tongue morphology impact feeding efficiency, pointing to evolutionary pathways that promote niche differentiation within nectar- feeding bat communities.

biophysics↗

bioRxiv2024

Testing for reciprocal trait influence in plant-frugivore interactions using generalized joint attribute modeling

Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in dispersal syndromes comprising both frugivore and plant traits that structure fruit consumption. Tests of this adaptive hypothesis, however, focus on traits of either fruits or frugivores but not both and often ignore within-species variation. To overcome these limitations, we analyze traits for the mutualistic ecological network comprising Carollia bats that feed on and disperse Piper seeds. For these analyses, we use generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of the adaptive hypothesis and indicating niche partitioning among Carollia bats, we find differential consumption of a suite of Piper species influenced by bat traits such as body size; however, Piper morphological traits had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such as Piper chemical bouquets, may explain the lack of association between bat Piper consumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant-frugivore interactions, providing a template for future trait analyses of plant-animal networks.

ecology↗

bioRxiv2023

Effects of habitat and fruit scent on the interactions between short-tailed fruit bats and Piper plants

Piper is a mega-diverse genus of pioneer plants that contributes to the maintenance and regeneration of tropical forests. With deforestation and climate change threatening forest ecosystems, understanding the mutualism between Piper and its seed dispersers becomes especially important. In the Neotropics, Carollia bats use olfaction to forage for Piper fruit and are a main disperser of Piper seeds via consumption and subsequent defecation during flight. In return, Piper fruits provide essential nutrients for Carollia year-round. There is evidence that the types and diversity of Piper frugivores are influenced by the primary habitat of different Piper species (forest, gap), with forest Piper depending more on bats for seed dispersal; however, this pattern has not been tested broadly. We aimed to characterize and compare the interactions between Carollia and Piper across forested and gap habitats, and further investigate whether differences in fruit traits relevant to bat foraging (i.e., scent) could underlie differences in Carollia-Piper interactions. We collected nightly acoustic ultrasonic recordings and 24h camera trap data in La Selva, Costa Rica across 12 species of Piper (6 forest, 6 gap) and integrated this information with data on Carollia diet and Piper fruit scent. Merging biomonitoring modalities allowed us to characterize ecological interactions in a hierarchical manner: from general activity and presence of bats, to visitations and inspections of plants, to acquisition and consumption of fruits. We found significant differences in Carollia-Piper interactions between forested and gap habitats; however, the type of biomonitoring modality (camera trap, acoustics, diet) influenced our ability to detect these differences. Forest Piper were exclusively visited by bats, whereas gap Piper had a more diverse suite of frugivores; the annual diet of Carollia, however, is dominated by gap Piper since these plants produce fruit year-round. We found evidence that fruit scent composition significantly differs between forest and gap Piper, which highlights the possibility that bats could be using chemical cues to differentially forage for gap versus forest Piper. By integrating studies of Piper fruit scent, plant visitation patterns, and Carollia diet composition, we paint a clearer picture of the ecological interactions between Piper and Carollia, and plant-animal mutualisms more generally.

ecology↗

bioRxiv2023

Size and locomotor ecology have differing effects on the external and internal morphologies of squirrel (Rodentia: Sciuridae) limb bones

Mammals exhibit a diverse range of limb morphologies that are associated with different locomotor ecologies and structural mechanics. Much remains to be investigated, however, about the combined effects of locomotor modes and scaling on the external shape and structural properties of limb bones. Here, we used squirrels (Sciuridae) as a model clade to examine the effects of locomotor mode and scaling on the external shape and structure of the two major limb bones, the humerus and femur. We quantified humeral and femoral morphologies using 3D geometric morphometrics and bone structure analyses on a sample of 76 squirrel species across their four major ecotypes. We then used phylogenetic generalized linear models to test how locomotor ecology, size, and their interaction influenced morphological traits. We found that size and locomotor mode exhibit different relationships with the external shape and structure of the limb bones, and that these relationships differ between the humerus and femur. External shapes of the humerus and, to a lesser extent, the femur are best explained by locomotor ecology rather than by size, whereas structures of both bones are best explained by interactions between locomotor ecology and scaling. Interestingly, the statistical relationships between limb morphologies and ecotype were lost when accounting for phylogenetic relationships among species under Brownian motion. That assuming Brownian motion confounded these relationships is not surprising considering squirrel ecotypes are phylogenetically clustered; our results suggest that humeral and femoral variation partitioned early between clades and their ecomorphologies were maintained to the present. Overall, our results show how mechanical constraints, locomotor ecology, and evolutionary history may enact different pressures on the shape and structure of limb bones in mammals.

evolutionary biology↗

bioRxiv2022

Scaling patterns of body plans differ among squirrel ecotypes

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 locomotory specializations, and describe the underlying morphological components that contribute to body shape variation 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 on these data, we found that 1) body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes; 2) only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs; and 3) the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape variation 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.

evolutionary biology↗

bioRxiv2022

Gliding towards an understanding of the origin of flight in bats

Bats are the only mammals capable of powered flight and have correspondingly specialized body plans, particularly in their limb morphology. The origin of bat flight is still not fully understood due to an uninformative fossil record but, from the perspective of a functional transition, it is widely hypothesized that bats evolved from gliding ancestors. Here, we test predictions of the gliding-to-flying hypothesis of the origin of bat flight by using phylogenetic comparative methods to model the evolution of forelimb and hindlimb traits on a dataset spanning four extinct bats and 231 extant mammals with diverse locomotor modes. Our results reveal that gliders exhibit adaptive trait optima (1) toward relatively elongate forelimbs that are intermediate between those of bats and non-gliding arborealists, and (2) toward relatively narrower but not longer hindlimbs that are intermediate between those of non-gliders and bats. We propose a hypothetical adaptive landscape based on limb length and width optimal trends derived from our modeling analyses. Our results support a hypothetical evolutionary pathway wherein glider-like postcranial morphology precedes a bat-like morphology adapted to powered-flight, setting a foundation for future developmental, biomechanical, and evolutionary research to test this idea.

evolutionary biology↗

bioRxiv2021

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

Mammalian olfactory receptors (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 repertoires 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 more specialized OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed leaf-nosed bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous versus duplicated receptors among Carollia species, and identified orthologous receptors and associated paralogs to explore the diversity and redundancy of the receptor gene repertoire. The most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two more generalist species (sowelli, perspicillata), but we discovered a few unique sets of ORs within C. castanea with exceptional redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants to an extent that the other species cannot. C. perspicillata, the species with the most generalist diet, had a larger diversity of functional receptors, suggesting the ability to detect a wider range of odorant molecules. The 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 plays a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants. Impact Statement--though it asks for 3-4 sentencesThe sense of smell is essential to how many animals detect food, yet few studies have demonstrated how dietary evolution has shaped olfactory receptor genes, which encode proteins that bind to environmental scent cues, including food odorants. We compared the evolutionary history of olfactory receptor repertoires in three co-occurring neotropical bat species along a spectrum of dietary specialization on the fruits of Piper plants. We found the more generalist species possessed a more diverse olfactory receptor profile, potentially reflecting an ability to detect more diverse arrays of fruit scent compounds, while the specialist had a narrower profile that demonstrated more redundancy. By introducing creative approaches to measure diversity in large gene families and connecting diet specialization and molecular diversity, this study makes an unprecedented contribution to evolutionary biology.

evolutionary biology↗

bioRxiv2019

A fruitful endeavor: scent cues and echolocation behavior used by Carollia castanea to find fruit

Frugivores have evolved sensory and behavioral adaptations that allow them to find ripe fruit effectively, but the relative importance of different senses in varying foraging scenarios is poorly known. Within Neotropical ecosystems, short-tailed fruit bats (Carollia: Phyllostomidae) are abundant nocturnal frugivores, relying primarily on plants of the genus Piper as a food resource. Previous research has demonstrated Carollia employ olfaction and echolocation to locate Piper fruit, but it is unknown how their sensory use and foraging decisions are influenced by the complex diversity of chemical cues that fruiting plants produce. Using wild C. castanea and their preferred food, Piper scintillans, we conducted behavioral experiments to test two main hypotheses: (1) foraging decisions in C. castanea are primarily driven by ripe fruit scent and secondarily by vegetation scent, and (2) C. castanea re-weight their sensory inputs to account for available environmental cues, such that bats rely more heavily on echolocation in the absence of adequate scent cues. Our results suggest that C. castanea requires olfactory information and relies almost exclusively on ripe fruit scent to make foraging attempts. Ripe fruit scent is chemically distinct from vegetation scent in P. scintillans, with a greater abundance of {beta}-caryophyllene, germacrene D and {beta}-elemene, and a few unique compounds. Although variation in echolocation call parameters was independent of scent cue presence, bats emitted longer and more frequent echolocation calls in trials where no fruit scent was present. Altogether, these results highlight the adaptations, plasticity, and potential constraints in the sensory system of neotropical fruit bats. SIGNIFICANCE STATEMENTLittle is known about the relative importance of different senses and which plant cues are most important for fruit location by frugivores. We conducted behavioral experiments on short-tailed fruit bats (Carollia castanea), which use a combination of olfaction and echolocation to find ripe fruit, and their preferred food source (Piper scintillans) to test (1) which plant scent cues drive food selection and (2) if bats alter their echolocation behaviors based on which scent cues are present. We find that C. castanea rely almost exclusively on ripe fruit scent to forage, and echolocate more frequently when fruit scent is absent. Ripe fruit scent is chemically different from vegetation scent in P. scintillans, potentially providing a clear signal of food availability to mutualistic bats. These results highlight the sensory adaptations and behavioral flexibility of fruit bats as they navigate the cues provided by fruiting plants.

ecology↗

bioRxiv2018

Anatomical diversification of a skeletal novelty in bat feet

Neomorphic, membrane-associated skeletal rods are found in disparate vertebrate lineages, but their evolution is poorly understood. Here we show that one of these elements--the calcar of bats (Chiroptera)--is a skeletal novelty that has anatomically diversified. Our comparisons of evolutionary models of calcar length and corresponding disparity-through-time analyses indicate that the calcar diversified early in the evolutionary history of Chiroptera, as bats systematically radiated after evolving the capacity for flight. We find interspecific variation in a variety of anatomical parameters of probable importance for calcar function, which suggests that adaptive advantages provided by the calcar led to its anatomical diversification. In addition to overall length, we find that the calcar varies among bats in its tissue composition, and a synovial joint is present at the articulation between the calcar and the calcaneus ankle bone in some species. This suggests the calcar has a kinematic functional role. Our results demonstrate that novel skeletal additions can become integrated into vertebrate body plans and subsequently evolve into a variety of forms, potentially impacting clade diversification by expanding the available morphological space into which organisms can evolve.

evolutionary biology↗