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University of Birmingham Quantifying the Completeness of the Bat Fossil University of Birmingham Quantifying the completeness of the bat fossil record Brown, Emily; Cashmore, Daniel; Simmons, Nancy; Butler, Richard DOI: 10.1111/pala.12426 License: Other (please specify with Rights Statement) Document Version Peer reviewed version Citation for published version (Harvard): Brown, E, Cashmore, D, Simmons, N & Butler, R 2019, 'Quantifying the completeness of the bat fossil record', Palaeontology, vol. 62, no. 5, pp. 757-776. https://doi.org/10.1111/pala.12426 Link to publication on Research at Birmingham portal Publisher Rights Statement: Checked for eligibility 10/01/2019 This is the peer reviewed version of the following article: Brown, E. E., Cashmore, D. D., Simmons, N. B. and Butler, R. J. (2019), Quantifying the completeness of the bat fossil record. Palaeontology. doi:10.1111/pala.12426, which has been published in final form at https://doi.org/10.1111/pala.12426. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving. General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 27. Sep. 2021 Page 1 of 109 Palaeontology 1 1 2 3 1 QUANTIFYING THE COMPLETENESS OF THE BAT FOSSIL RECORD 4 5 6 2 EMILY E. BROWN1, DANIEL D. CASHMORE1, NANCY B. SIMMONS2, RICHARD J. 7 8 1 9 3 BUTLER 10 11 1 12 4 School of Geography, Earth and Environmental Sciences, University of Birmingham, 13 14 5 Edgbaston, Birmingham, B15 2TT, UK 15 16 17 6 2Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural 18 19 7 History, New York, New York, 10024, USA 20 21 22 8 23 24 25 9 Corresponding authors: 26 27 28 10 Emily E. Brown ([email protected]), Daniel D. Cashmore 29 30 11 ([email protected]) 31 32 33 12 34 35 36 13 37 38 39 14 40 41 42 15 43 44 45 16 46 47 48 17 49 50 51 18 52 53 54 19 55 56 57 20 58 59 60 Palaeontology Palaeontology Page 2 of 109 2 1 2 3 21 Abstract: Bats (Chiroptera) are one of the most successful extant mammalian orders, 4 5 6 22 uniquely capable of powered flight and laryngeal echolocation. The timing and evidence for 7 8 23 evolution of their novel adaptations have been difficult to ascertain from the fossil record due 9 10 24 to chronological gaps and the fragmentary nature of most fossil bat material. Here, we 11 12 quantify the quality of the bat fossil record using skeletal and character completeness metrics, 13 25 14 15 26 which respectively document for each taxon what proportion of a complete skeleton is 16 17 27 preserved, and the proportion of phylogenetic characters that can be scored. Completeness 18 19 28 scores were collected for 441 valid fossil bat species in 167 genera from the Eocene to 20 21 22 29 Pleistocene. All metrics record similar temporal patterns: peak completeness in the Lutetian 23 24 30 stage reflects the presence of Lagerstätten, while subsequent stages have very low 25 26 31 completeness, excepting an Aquitanian high and a Pleistocene peak in skeletal completeness. 27 28 29 32 Bat completeness is not correlated with intensity of sampling through geological time but has 30 31 33 a weak negative correlation with publication date. There is no correlation between taxonomic 32 33 34 richness and completeness, as the bat record predominately consists of diagnostic but isolated 34 35 teeth. Consequently, bat skeletal completeness is the lowest of any previously assessed 36 35 37 38 36 tetrapod group, but character completeness is similar to parareptiles and birds. Bats have 39 40 37 significantly higher character completeness in the northern hemisphere, likely due to 41 42 38 heightened historical interest and presence of Lagerstätten. Taxa derived from caves are more 43 44 45 39 complete than those from fluviolacustrine and marine deposits, but do not preserve highly 46 47 40 complete specimens. 48 49 50 41 51 52 53 42 54 55 56 43 KEYWORDS: Chiroptera, completeness metrics, Cenozoic, caves, Lagerstätten, sampling 57 58 44 bias 59 60 Palaeontology Page 3 of 109 Palaeontology 3 1 2 3 45 4 5 6 46 INTRODUCTION 7 8 9 47 Bats (Chiroptera) are one of the most successful and diverse orders of extant mammals. They 10 11 12 48 have a nearly global distribution, a varied range of body sizes, are known to have 13 14 49 insectivorous, carnivorous, frugivorous, nectarivorous and hematophagous diets, and with 15 16 50 nearly 1400 species, bats account for ~20% of all extant mammalian species (Wilson and 17 18 51 Reeder 2005; Shi and Rabosky 2015; Tsang et al. 2015; Simmons and Cirranello 2018). Bats 19 20 21 52 are the only living mammals, and one of only three vertebrate groups (along with pterosaurs 22 23 53 and birds), that are capable of true self-powered flight (Padian 1985; Norberg 1990; Templin 24 25 54 2000; Dudley et al. 2007; Swartz et al. 2012). The extreme elongation of their forelimb digits 26 27 28 55 plus development of a thin interconnected membrane (patagium) gives bats a unique body 29 30 56 plan (Swartz et al. 1992; Swartz and Middleton 2008). They are also the only mammals 31 32 57 capable of sophisticated laryngeal echolocation, in which they emit high-frequency sounds 33 34 35 58 and interpret returning echoes to perceive their environment, enabling ‘visualisation’ in 36 37 59 complete darkness (Arita and Fenton 1997; Teeling et al. 2012). Echolocation is the 38 39 60 dominant mode of sensory perception in all bat families, with the exception of many of the 40 41 61 fruit bats (Pteropodidae), which instead rely primarily on vision and olfaction (Arita and 42 43 44 62 Fenton 1997; Boonman et al. 2013). Understanding the timing of and mechanisms 45 46 63 underpinning the evolution of the unique adaptations of bats is an important goal of 47 48 64 evolutionary biologists. 49 50 51 65 Monophyly of Chiroptera is consistently strongly supported by morphological and 52 53 54 66 molecular analyses (e.g. Springer et al. 2001; Teeling et al. 2005; Song et al. 2012; Meredith 55 56 67 et al. 2011; O’Leary et al. 2013; Tsagkogeorga et al. 2013; Lei and Dong 2016). The relative 57 58 68 position of Chiroptera within the placental mammal tree has been the subject of debate, but it 59 60 Palaeontology Palaeontology Page 4 of 109 4 1 2 3 69 is now uniformly placed within Laurasiatheria (Springer et al. 2001; Teeling et al. 2002; 4 5 6 70 Song et al. 2012; Meredith et al. 2013; O’Leary et al. 2013; Tsagkogeorga et al. 2013; 7 8 71 Halliday et al. 2017). Chiroptera is divided into two suborders, Yinpterochiroptera and 9 10 72 Yangochiroptera, based on morphological, molecular, and genomic evidence (Teeling et al. 11 12 2002; Meredith et al. 2013; Tsagkogeorga et al. 2013; Lei and Dong 2016). These suborders 13 73 14 15 74 are not distinguished by echolocation ability (both clades contain laryngeal echolocators), and 16 17 75 differ from the traditional division of bats into Megachiroptera and Microchiroptera (Teeling 18 19 76 et al. 2005; O’Leary et al. 2013). Time-calibrated molecular and genomic phylogenies 20 21 22 77 indicate that bats evolved shortly after the Cretaceous-Palaeogene (K-Pg) boundary, with the 23 24 78 split of Yinpterochiroptera and Yangochiroptera occurring around 63 million years ago (Ma) 25 26 79 (Teeling et al. 2005; Lei and Dong 2016). Analyses combining morphological and molecular 27 28 29 80 data similarly indicate an early origin around the K-Pg boundary, but suggest that the bat 30 31 81 crown group diversified later, perhaps 57 Ma (O’Leary et al. 2013). Fossils could potentially 32 33 82 provide the critical direct evidence of these relationships and divergence dates. However, the 34 35 fossil record does not shed light on earliest history of bat evolution as the first unambiguous 36 83 37 38 84 bats occur only in the early Eocene, leaving a 10-million-year gap between the apparent 39 40 85 origin of the lineage and the first recognizable bat fossils (Gunnell and Simmons 2005). 41 42 43 86 Despite existence of several well-known complete skeletons, the fossil record of bats 44 45 87 has generally been regarded as being exceptionally poor (Gunnell and Simmons 2005; 46 47 48 88 Teeling et al.
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