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Integrated Fossil and Molecular Data Reconstruct Bat Echolocation

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Integrated Fossil and Molecular Data Reconstruct Bat Echolocation Integrated fossil and molecular data reconstruct bat echolocation Mark S. Springer†‡, Emma C. Teeling†§, Ole Madsen¶, Michael J. Stanhope§ʈ, and Wilfried W. de Jong¶** †Department of Biology, University of California, Riverside, CA 92521; §Queen’s University of Belfast, Biology and Biochemistry, 97 Lisburn Road, Belfast BT9 7BL, United Kingdom; ¶Department of Biochemistry, University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands; ʈBioinformatics, SmithKline Beecham Pharmaceuticals, 1250 South Collegeville Road, UP1345, Collegeville, PA 19426; and **Institute for Biodiversity and Ecosystem Dynamics, 1090 GT Amsterdam, The Netherlands Edited by David Pilbeam, Harvard University, Cambridge, MA, and approved March 26, 2001 (received for review November 21, 2000) Molecular and morphological data have important roles in illumi- tulates a sister-group relationship between flying lemurs and bats nating evolutionary history. DNA data often yield well resolved (6). Although some authors have questioned bat monophyly phylogenies for living taxa, but are generally unattainable for based on evidence from the penis and nervous system (7, 8), the fossils. A distinct advantage of morphology is that some types of bulk of morphological data supports bat monophyly (9). Among morphological data may be collected for extinct and extant taxa. living Chiroptera, morphological data provide strong support for Fossils provide a unique window on evolutionary history and may the reciprocal monophyly of megachiropterans (Old World fruit preserve combinations of primitive and derived characters that are bats), all of which lack laryngeal echolocation, and microchi- not found in extant taxa. Given their unique character complexes, ropterans, all of which possess laryngeal echolocation (6, 10, 11). fossils are critical in documenting sequences of character transfor- In a total evidence analysis that combined 180 morphological mation over geologic time and may elucidate otherwise ambigu- and 12 restriction site characters, Simmons (10) obtained 100% ous patterns of evolution that are not revealed by molecular data bootstrap support for the monophyly of extant microbats. alone. Here, we employ a methodological approach that allows for The oldest fossil bats are from early Eocene deposits in Africa, the integration of molecular and paleontological data in decipher- Australia, Europe, and North America. Of the eight currently ing one of the most innovative features in the evolutionary history recognized genera from the early Eocene, four (Icaronycteris, EVOLUTION of mammals—laryngeal echolocation in bats. Molecular data Archaeonycteris, Hassianycteris, Palaeochiropteryx) are known alone, including an expanded data set that includes new sequences from relatively complete skeletons (6). Simmons and Geisler (6) for the A2AB gene, suggest that microbats are paraphyletic but do expanded the data set of Simmons (10) to include 208 characters not resolve whether laryngeal echolocation evolved indepen- (195 morphological); they also added Icaronycteris, Archaeonyc- dently in different microbat lineages or evolved in the common teris, Hassianycteris, and Palaeochiropteryx to this matrix. Based ancestor of bats and was subsequently lost in megabats. When on an extensive set of phylogenetic analyses, they concluded that scaffolds from molecular phylogenies are incorporated into parsi- the Eocene taxa constitute a consecutive series of sister-taxa to mony analyses of morphological characters, including morpholog- a monophyletic crown-group Microchiroptera. Furthermore, the ical characters for the Eocene taxa Icaronycteris, Archaeonycteris, Eocene fossils exhibit anatomical features that suggest the Hassianycteris, and Palaeochiropteryx, the resulting trees suggest occurrence of laryngeal echolocation in these taxa. Simmons and that laryngeal echolocation evolved in the common ancestor of fossil and extant bats and was subsequently lost in megabats. Geisler (6) thus concluded that laryngeal echolocation evolved Molecular dating suggests that crown-group bats last shared a only once in the evolutionary history of Chiroptera. common ancestor 52 to 54 million years ago. Molecular data validate the conclusion that the order Chi- roptera is monophyletic (12, 13). There are also unexpected results from molecular studies. First, bats are not closely related oth molecular and morphological data have important roles to other archontans (14–17). Rather, bats are members of the Bin elucidating evolutionary history and phylogeny. Advan- clade Laurasiatheria (16, 18), which also includes eulipotyphlan tages of molecular data include the large number of characters insectivores, pangolins, carnivores, perissodactyls, and cetartio- that are available (1) as well as sophisticated models of sequence dactyls. This implies that putative synapomorphies of Volitantia evolution that may be used in phylogenetic analyses (2). How- are instead homoplasic features in Chiroptera and Dermoptera. ever, in most instances it has not been possible to obtain DNA Molecular data also challenge microbat monophyly and instead sequences for fossil taxa. In contrast, certain types of morpho- suggest that microbats are paraphyletic, with rhinolophoids more logical data may be collected for both fossil and extant taxa. closely related to megabats than to other microbats (15, 19, 20). Fossils provide a unique window on evolutionary history and New sequence data presented below provide increased support often preserve combinations of primitive and derived characters for this hypothesis. Microbat paraphyly implies that complex that are not found in extant taxa (3). Given their unique laryngeal echolocation either evolved independently in rhinolo- character complexes, fossils are critical in documenting se- quences of character transformation over geologic time (4). phoids and other microbats or evolved in the ancestor of Morphological evidence from fossils may reveal patterns of Chiroptera with subsequent loss in megabats. Given these com- evolution that are not apparent from molecular phylogenies peting hypotheses, which are equally parsimonious in the context alone. Below, we illustrate a methodological approach that of molecular phylogenies that have only included living taxa, we allows for the integration of molecular and paleontological data in deciphering one of the most innovative features in This paper was submitted directly (Track II) to the PNAS office. the evolutionary history of mammals—laryngeal echolocation Abbreviations: ML, maximum likelihood; MP, maximum parsimony; ts͞tv, transition to in bats. transversion ratio. Interfamilial relationships among bats, as well as relationships Data deposition: The sequences reported in this paper have been deposited in the GenBank of the order Chiroptera to other eutherian orders, have been database (accession nos. AF337537–AF337543). investigated with both morphological and molecular data. Mor- ‡To whom reprint requests should be addressed. E-mail: [email protected]. phological data suggest that bats are in the superordinal group The publication costs of this article were defrayed in part by page charge payment. This Archonta (5), which also includes primates, tree shrews, and article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. flying lemurs. Within Archonta, the Volitantia hypothesis pos- §1734 solely to indicate this fact. www.pnas.org͞cgi͞doi͞10.1073͞pnas.111551998 PNAS ͉ May 22, 2001 ͉ vol. 98 ͉ no. 11 ͉ 6241–6246 Downloaded by guest on September 24, 2021 investigated the origin and evolutionary history of laryngeal echolocation in microbats by using an integrated approach that used both molecular phylogenies and morphological data for living and extinct taxa. Molecular phylogenies were used to construct a backbone phylogenetic constraint, or scaffold, for a subset of extant bat families͞subfamilies for which DNA phy- logenies are available (see Methods). Parsimony analyses with the morphological data set of Simmons and Geisler (6), in conjunction with the molecular scaffolds, provide support for the hypothesis that laryngeal echolocation evolved in the common ancestor of Chiroptera and was subsequently lost in megabats. Methods New sequences for Ϸ1.3 kb of the A2AB gene were amplified and sequenced as described (16, 21) for Megaderma lyra (Gen- Bank accession no. AF337537), Hipposideros commersoni (AF337538), Pteropus rayneri (AF337539), Myotis daubentoni (AF337540), Tonatia bidens (AF337541), Tadarida brasiliensis (AF337542), and Taphozous sp. (AF337543). Additional A2AB sequences were obtained from GenBank for one megabat (Cynopterus sphinx; AJ251181) and the outgroups Rattus norve- gicus (M32061), Homo sapiens (M34041), Felis catus (AJ251174), and Cynocephalus variegatus (AJ251182). The outgroups in- Fig. 1. Maximum likelihood phylogram (HKY85 model with a ⌫ distribution cluded one laurasiatherian (Felis) and two archontans (Homo, of rates) based on the 9427-bp data set (Ϫln likelihood ϭ 48718.269). Scale bar Cynocephalus) based on alternate views that bats are either corresponds to 5% sequence divergence. ML bootstrap support values are members of Laurasiatheria or Archonta. The A2AB sequences shown adjacent to or above branches. Support values with other methods of analysis are given in Table 1. were aligned by using CLUSTAL W (22). Phylogenetic analyses were performed for A2AB sequences alone as well as for a concatenation of sequences that included published sequences two pairs of sister taxa in
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