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

ABSTRACT: Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adaptive zone shifts in bat skull shape. Here we report that, while disparity was established early, bat skull evolution is best described by multiple adaptive zone shifts. Shifts are partially decoupled between the cranium and mandible, with cranial evolution more strongly driven by echolocation than diet. Phyllostomidae, a trophic adaptive radiation, exhibits more adaptive zone shifts than all other families combined. This pattern was potentially driven by ecological opportunity and facilitated by a shift to intermediate cranial shapes compared to oral-emitters and other nasal emitters.

SUBMITTER: Arbour JH

PROVIDER: S-EPMC6497661 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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

Arbour Jessica H JH Curtis Abigail A AA Santana Sharlene E SE

Nature communications 20190502 1

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adapt ...[more]

PMID: 31048713

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Project description:All organisms have specialized systems to sense their environment. Most bat species use echolocation for navigation and foraging, but which and how ecological factors shaped echolocation call diversity remains unclear for the most diverse clades, including the adaptive radiation of neotropical leaf-nosed bats (Phyllostomidae). This is because phyllostomids emit low-intensity echolocation calls and many inhabit dense forests, leading to low representation in acoustic surveys. We present a field-collected, echolocation call dataset spanning 35 species and all phyllostomid dietary guilds. We analyze these data under a phylogenetic framework to test the hypothesis that echolocation call design and parameters are specialized for the acoustic demands of different diets, and investigate the contributions of phylogeny and body size to echolocation call diversity. We further link call parameters to dietary ecology by contrasting minimum detectable prey size estimates (MDPSE) across species. We find phylogeny and body size explain a substantial proportion of echolocation call parameter diversity, but most species can be correctly assigned to taxonomic (61%) or functional (77%) dietary guilds based on call parameters. This suggests a degree of acoustic ecological specialization, albeit with interspecific similarities in call structure. Theoretical MDPSE are greatest for omnivores and smallest for insectivores. Omnivores significantly differ from other dietary guilds in MDPSE when phylogeny is not considered, but there are no differences among taxonomic dietary guilds within a phylogenetic context. Similarly, predators of non-mobile/non-evasive prey and predators of mobile/evasive prey differ in estimated MDPSE when phylogeny is not considered. Phyllostomid echolocation call structure may be primarily specialized for overcoming acoustic challenges of foraging in dense habitats, and then secondarily specialized for the detection of food items according to functional dietary guilds. Our results give insight into the possible ecological mechanisms shaping the diversity of sensory systems, and their reciprocal influence on resource use.

Project description:Phylogeny, ecology, and sensorial constraints are thought to be the most important factors influencing echolocation call design in bats. The Molossidae is a diverse bat family with a majority of species restricted to tropical and subtropical regions. Most molossids are specialized to forage for insects in open space, and thus share similar navigational challenges. We use an unprecedented dataset on the echolocation calls of 8 genera and 18 species of New World molossids to explore how habitat, phylogenetic relatedness, body mass, and prey perception contribute to echolocation call design. Our results confirm that, with the exception of the genus Molossops, echolocation calls of these bats show a typical design for open space foraging. Two lines of evidence point to echolocation call structure of molossids reflecting phylogenetic relatedness. First, such structure is significantly more similar within than among genera. Second, except for allometric scaling, such structure is nearly the same in congeneric species. Despite contrasting body masses, 12 of 18 species call within a relatively narrow frequency range of 20 to 35 kHz, a finding that we explain by using a modeling approach whose results suggest this frequency range to be an adaptation optimizing prey perception in open space. To conclude, we argue that the high variability in echolocation call design of molossids is an advanced evolutionary trait allowing the flexible adjustment of echolocation systems to various sensorial challenges, while conserving sender identity for social communication. Unraveling evolutionary drivers for echolocation call design in bats has so far been hampered by the lack of adequate model organisms sharing a phylogenetic origin and facing similar sensorial challenges. We thus believe that knowledge of the echolocation call diversity of New World molossid bats may prove to be landmark to understand the evolution and functionality of species-specific signal design in bats.

Dataset Information

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

Publications

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

Similar Datasets

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