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Bat Skull Evolution: the Impact of Echolocation

Giacomini, G (2020) Bat Skull Evolution: the Impact of Echolocation. Doctoral thesis, Liverpool John Moores University.

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Abstract

Morphological adaptations of the mammalian skull are influenced by a variety of functional, environmental and behavioural factors. Skulls of echolocating species, such as bats, also face the challenge of optimizing sound emission and propagation. A strong association between bat skull morphology and feeding behaviour has been suggested previously (in particular for the Phyllostomidae family). Morphological variation related to other drivers of adaptation (in particular echolocation) remains understudied. In this thesis, I investigated the relationship between bat skull morphology (i.e., size and shape) and functional traits (i.e., feeding and echolocation) with a focus on the echolocation adaptations. I applied geometric morphometrics on data acquired from 3D digital models of bat skulls reconstructed with photogrammetry and μCT scan techniques. The power and limitations of photogrammetry have not been fully explored for studies of evolutionary processes of small animals. As such, I firstly demonstrated the reliability of photogrammetry for the reconstruction of 3D digital models of bat skulls by evaluating its potential for evolutionary morphology studies at the interspecific level. I found that the average distance between meshes reconstructed with different techniques (i.e., photogrammetry, μCT or laser scan) was 0.037 mm (0.25% of total skull length). Levels of random error (repeatability and Procrustes variance) were similar in all techniques and no systematic error was observed. Therefore, the same biological conclusions are obtained regardless of the reconstruction technique employed. I subsequently assessed variation in skull morphology, with respect to ecological group (i.e., diet and emission type) and functional measures (i.e., bite force, masticatory muscles and echolocation characteristics), using phylogenetic comparative methods. I found that skull diversification among bat families is mainly driven by sound emission type (i.e., nasal and oral) and broad diatary preferences. Feeding parameters (i.e., bite force and masticatory muscles) influence the shape and size of all families studied and not only in phyllostomids: bigger species generate stronger bites and species with a short rostrum generate higher bite forces relative to their body size. Sensory parameters (i.e., echolocation characteristics) scale with skull size and correlate with skull shape in insectivorous species. I estimated the relative effects of feeding and sensory functional demands on skull size and shape variation and found comparable effects within the insectivorous species. Echolocation and feeding functions appear to constrain the same skull shape characteristics (i.e., rostrum length) in insect-eating species indicating a possible functional trade-off. These species possibly underwent strong selection on skull morphology due to the (almost) exclusive use of echolocation to pursuit rapidly moving prey. Additionally, echolocation signals in bats vary in call design (i.e., number of harmonics, constant frequency, quasi-constant frequency and frequency modulation components) and some have evolved multiple times in different lineages. Therefore, I tested the effect of emission type and call design on the relationship between peak frequency and skull morphology within a broad taxonomic context (219 species). Skull morphology (i.e., size and shape) of constant frequency nasal emitting species is strongly associated with peak frequency to amplify the sound through resonance effect within the nasal chambers. Despite no resonance effect being known for oral emitting species, skull shape variation also correlates with peak frequency in these species. Spatial and mechanical demands of echolocating muscles might mould the skull shape during ontogenesis of oral emitting species: the correlation between peak frequency and shape may result from an indirect mechanical effect. Interestingly, the skull shape of some non-insectivorous species (i.e., frugivorous phyllostomids) also shows an evolutionary correlation with peak frequency. This suggests that peak frequency is still constraining skull shape of phyllostomid bats or, as phyllostomids probably evolved from an insectivorous ancestor, the adaptations to echolocation are evolutionary conservative. This thesis advances our knowledge of bat skull adaptation to echolocation and encourages future evolutionary studies to focus more on under-studied echolocation parameters.

Item Type: Thesis (Doctoral)
Uncontrolled Keywords: Geometric Morphometrics; Evolutionary Biology
Subjects: Q Science > QL Zoology
Divisions: Biological & Environmental Sciences (new Sep 19)
Date Deposited: 03 Apr 2020 08:43
Last Modified: 03 Apr 2020 08:43
DOI or Identification number: 10.24377/LJMU.t.00012640
Supervisors: Meloro, C and Brown, R
URI: http://researchonline.ljmu.ac.uk/id/eprint/12640

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