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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.more » « less
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Abstract Comparative studies are a common way to address large‐scale questions in sensory biology. For studies that investigate olfactory abilities, the most commonly used metric is olfactory bulb size. However, recent work has called into question the broad‐scale use of olfactory bulb size. In this paper, we use three neuroanatomical measures with a more mechanistic link to olfactory function (number of olfactory sensory neurons (OSNs), number of mitral cells (MCs), and number of glomeruli) to ask how species with different diets may differ with respect to olfactory ability. We use phyllostomid bats as our study system because behavioral and physiological work has shown that fruit‐ and nectar‐feeding phyllostomids rely on odors for detecting, localizing, and assessing potential foods, while insect‐eating species do not. Therefore, we predicted that fruit‐ and nectar‐feeding bats would have larger numbers of these three neuroanatomical measures than insect‐eating species. In general, our results supported the predictions. We found that fruit‐eaters had greater numbers of OSNs and glomeruli than insect‐eaters, but we found no difference between groups in number of MCs. We also examined the allometric relationship between the three neuroanatomical variables and olfactory bulb volume, and we found isometry in all cases. These findings lend support to the notion that neuroanatomical measures can offer valuable insights into comparative olfactory abilities, and suggest that the size of the olfactory bulb may be an informative parameter to use at the whole‐organism level.
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Abstract Marsupial neonates are born at an earlier developmental stage than placental mammals, but the rapid development of their forelimbs and cranial skeleton allows them to climb to the pouch, begin suckling and complete their development
ex utero . The mechanical environment in which marsupial neonates develop is vastly different from that of placental neonates, which exhibit a more protracted development of oral muscles and bones. This difference in reproductive strategy has been theorized to constrain morphological evolution in the oral region of marsupials. Here, we use 3D morphometrics to characterize one of these oral bones, the lower jaw (dentary), and assess modularity (pattern of covariation among traits), morphological disparity and rates of morphological evolution in two clades of carnivorous mammals: the marsupial Dasyuromorphia and placental fissiped Carnivora. We find that dasyuromorph dentaries have fewer modules than carnivorans and exhibit tight covariation between the angular and coronoid processes, the primary attachment sites for jaw‐closing muscles. This pattern of modularity may result from the uniform action of muscles on the developing mandible during suckling. Carnivorans are free from this constraint and exhibit a pattern of modularity that more strongly reflects genetic and developmental signals of trait covariation. Alongside differences in modularity, carnivorans exhibit greater disparity and faster rates of morphological evolution compared with dasyuromorphs. Taken together, this suggests dasyuromorphs have retained a signal of trait covariation that reflects the outsized influence of muscular force during early development, a feature that may have impacted the ability of marsupial carnivores to explore specialized regions of morphospace. -
Abstract Sensory organs must develop alongside the skull within which they are largely encased, and this relationship can manifest as the skull constraining the organs, organs constraining the skull, or organs constraining one another in relative size. How this interplay between sensory organs and the developing skull plays out during the evolution of sensory diversity; however, remains unknown. Here, we examine the developmental sequence of the cochlea, the organ responsible for hearing and echolocation, in species with distinct diet and echolocation types within the ecologically diverse bat super‐family Noctilionoidea. We found the size and shape of the cochlea largely correlates with skull size, with exceptions of
Pteronotus parnellii , whose high duty cycle echolocation (nearly constant emission of sound pulses during their echolocation process allowing for detailed information gathering, also called constant frequency echolocation) corresponds to a larger cochlear and basal turn, andMonophyllus redmani , a small‐bodied nectarivorous bat, for which interactions with other sensory organs restrict cochlea size. Our findings support the existence of developmental constraints, suggesting that both developmental and anatomical factors may act synergistically during the development of sensory systems in noctilionoid bats. -
Bats are famous for using their hearing to explore their environments, yet fewer people are aware that these flying mammals have both good night and daylight vision. Some bats can even see in color thanks to two light-sensitive proteins at the back of their eyes: S-opsin which detects blue and ultraviolet light and L-opsin which detects green and red light. Many species of bat, however, are missing one of these proteins and cannot distinguish any colors; in other words, they are completely color-blind. Some bat species found in Central and South America have independently lost their ability to see blue-ultraviolet light and have thus also lost their color vision. These bats have diverse diets – ranging from insects to fruits and even blood – and being able to distinguish color may offer an advantage in many of their activities, including hunting or foraging. The vision genes in these bats, therefore, give scientists an opportunity to explore how a seemingly important trait can be lost at the molecular level. Sadier, Davies et al. now report that S-opsin has been lost more than a dozen times during the evolutionary history of these Central and South American bats. The analysis used samples from 55 species, including animals caught from the wild and specimens from museums. As with other proteins, the instructions encoded in the gene sequence for S opsin need to be copied into a molecule of RNA before they can be translated into protein. As expected, S-opsin was lost several times because of changes in the gene sequence that disrupted the formation of the protein. However, at several points in these bats’ evolutionary history, additional changes have taken place that affected the production of the RNA or the protein, without an obvious change to the gene itself. This finding suggests that other studies that rely purely on DNA to understand evolution may underestimate how often traits may be lost. By capturing ‘evolution in action’, these results also provide a more complete picture of the molecular targets of evolution in a diverse set of bats.more » « less
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Abstract Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye‐expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant‐based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and—unusually for echolocating bats—often have large, well‐developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar‐feeding lineages and the subfamily Stenodermatinae of fig‐eating bats fine‐tuning pre‐existing visual adaptations for specialized purposes.