Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats

Arbour, Jessica H.; Curtis, Abigail; Santana, Sharlene E.

doi:10.1038/s41467-019-09951-y

Cited by 106 publications

(135 citation statements)

References 75 publications

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“…The main dimension of phyllostomid cranial evolution is the length of the skull and snout, a morphological characteristic important to phyllostomid feeding ecology [5,10,15,54]. The faces of phyllostomids show a full range of phenotypes from the extremely shortened-faces of the fruit bats to the highly elongated faces of the nectarfeeding bats, which encompass the majority of variation based on principal components (PC) analysis (Fig.…”

Section: Discussionmentioning

confidence: 99%

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

Camacho

Moon

Smith

et al. 2020

EvoDevo

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Background: Skull diversity in the neotropical leaf-nosed bats (Phyllostomidae) evolved through a heterochronic process called peramorphosis, with underlying causes varying by subfamily. The nectar-eating (subfamily Glossophaginae) and blood-eating (subfamily Desmondontinae) groups originate from insect-eating ancestors and generate their uniquely shaped faces and skulls by extending the ancestral ontogenetic program, appending new developmental stages and demonstrating peramorphosis by hypermorphosis. However, the fruit-eating phyllostomids (subfamilies Carollinae and Stenodermatinae) adjust their craniofacial development by speeding up certain developmental processes, displaying peramorphosis by acceleration. We hypothesized that these two forms of peramorphosis detected by our morphometric studies could be explained by differential growth and investigated cell proliferation during craniofacial morphogenesis. Results: We obtained cranial tissues from four wild-caught bat species representing a range of facial diversity and labeled mitotic cells using immunohistochemistry. During craniofacial development, all bats display a conserved spatiotemporal distribution of proliferative cells with distinguishable zones of elevated mitosis. These areas were identified as modules by the spatial distribution analysis. Ancestral state reconstruction of proliferation rates and patterns in the facial module between species provided support, and a degree of explanation, for the developmental mechanisms underlying the two models of peramorphosis. In the long-faced species, Glossophaga soricina, whose facial shape evolved by hypermorphosis, cell proliferation rate is maintained at lower levels and for a longer period of time compared to the outgroup species Miniopterus natalensis. In both species of studied short-faced fruit bats, Carollia perspicillata and Artibeus jamaicensis, which evolved under the acceleration model, cell proliferation rate is increased compared to the outgroup. Conclusions: This is the first study which links differential cellular proliferation and developmental modularity with heterochronic developmental changes, leading to the evolution of adaptive cranial diversity in an important group of mammals.

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Section: Discussionmentioning

confidence: 99%

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

Camacho

Moon

Smith

et al. 2020

EvoDevo

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“…In concert with ecological diversification, noctilionoids evolved highly diverse sensory modalities, including infrared thermal radiation detection in vampire bats, high duty cycle (HDC) echolocation in the Pteronotus parnellii species complex (family Mormoopidae), and inferred ultraviolet (UV) perception in some nectar‐feeding lineages (Gracheva et al., 2011; Smotherman & Guillen‐Servent, 2008; Winter, Lopez, & Helversen, 2003). However, most previous research has focused on the relationship between noctilionoid diet and morphology (Arbour, Curtis, & Santana, 2019; Dumont et al., 2012; Rojas et al., 2011), with analyses linking foraging modes and molecular adaptations of sensory systems in this clade having only recently started (Hayden et al., 2014; Hong & Zhao, 2014; Sadier et al., 2018; Yohe et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

Foraging shifts and visual preadaptation in ecologically diverse bats

et al. 2020

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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.

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“…These observations may have two explanations. Arbour et al [78] found that echolocation related to an early lineage of species had a greater contribution than diet to the evolution of the cranium in bats. Moreover, the skull morphology in carnivores and marsupials are strongly influenced by phylogeny, especially in felids, ursids, and canids [26,79,80].…”

Section: The Relationship Between Skull Morphology With Bite Force Anmentioning

confidence: 99%

Correlation of skull morphology and bite force in a bird-eating bat (Ia io; Vespertilionidae)

et al. 2020

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Background: Genetic and ecological factors influence morphology, and morphology is compatible with function. The morphology and bite performance of skulls of bats show a number of characteristic feeding adaptations. The great evening bat, Ia io (Thomas, 1902), eats both insects and birds (Thabah et al. J Mammal 88: 728-735, 2007), and as such, it is considered to represent a case of dietary niche expansion from insects to birds. How the skull morphology or bite force in I. io are related to the expanded diet (that is, birds) remains unknown. We used three-dimensional (3D) geometry of the skulls and measurements of bite force and diets from I. io and 13 other species of sympatric or closely related bat species to investigate the characteristics and the correlation of skull morphology and bite force to diets.Results: Significant differences in skull morphology and bite force among species and diets were observed in this study. Similar to the carnivorous bats, bird-eaters (I. io) differed significantly from insectivorous bats; I. io had a larger skull size, taller crania, wider zygomatic arches, shorter but robust mandibles, and larger bite force than the insectivores. The skull morphology of bats was significantly associated with bite force whether controlling for phylogeny or not, but no significant correlations were found between diets and the skulls, or between diets and residual bite force, after controlling for phylogeny.Conclusions: These results indicated that skull morphology was independent of diet, and phylogeny had a greater impact on skull morphology than diet in these species. The changes in skull size and morphology have led to variation in bite force, and finally different bat species feeding on different foods. In conclusion, I. io has a larger skull size, robust mandibles, shortened dentitions, longer coronoid processes, expanded angular processes, low condyles, and taller cranial sagittal crests, and wider zygomatic arches that provide this species with mechanical advantages; their greater bite force may help them use larger and hard-bodied birds as a dietary component.

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Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats

Cited by 106 publications

References 75 publications

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

Foraging shifts and visual preadaptation in ecologically diverse bats

Correlation of skull morphology and bite force in a bird-eating bat (Ia io; Vespertilionidae)

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