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PHYLOGENY OF PHYLLOSTOMID BATS (MAMMALIA: CHIROPTERA): DATA FROM DIVERSE MORPHOLOGICAL SYSTEMS, SEX CHROMOSOMES, AND RESTRICTION SITES ANDREA L. WETTERER Graduate Fellow, Division of Vertebrate Zoology, Department of Mammalogy, American Museum of Natural History; Graduate Student, Program in Ecology and Evolutionary Biology Columbia University MATTHEW V. ROCKMAN Intern, Division of Vertebrate Zoology, Department of Mammalogy, American Museum of Natural History NANCY B. SIMMONS Associate Curator, Division of Vertebrate Zoology, Department of Mammalogy, American Museum of Natural History BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY Number 248, 200 pages, 66 ®gures, 8 tables, 4 appendices Issued March 1, 2000 Price: $17.40 a copy Copyright q American Museum of Natural History 2000 ISSN 0003-0090 CONTENTS Abstract ....................................................................... 4 Introduction .................................................................... 5 Historical Background ........................................................... 7 Phyllostomid Classi®cation from 1758 to Present ................................. 7 Summary ................................................................... 35 Materials and Methods ......................................................... 36 Sampling and Character Coding ............................................... 36 Assessing Congruence Among Data Sets ....................................... 39 Phylogenetic Analyses ....................................................... 41 Character Descriptions .......................................................... 42 Pelage and Integument ....................................................... 46 Skull and Dentition .......................................................... 67 Postcranium ................................................................. 87 Hyoid Apparatus ............................................................ 93 Tongue .................................................................... 101 Digestive Tract ............................................................. 115 Reproductive Tract .......................................................... 116 Brain ...................................................................... 119 Sex Chromosomes .......................................................... 122 Restriction Sites ............................................................ 122 EcoRI-De®ned DNA Repeat ................................................. 124 Results ...................................................................... 125 Taxonomic Congruence Analysis ............................................. 125 Pelage and Integument .................................................... 125 Skull and Dentition ....................................................... 125 Postcranium ............................................................. 125 Hyoid Apparatus ......................................................... 125 Tongue .................................................................. 129 Digestive Tract ........................................................... 131 Reproductive Tract ....................................................... 131 Brain ................................................................... 131 Sex Chromosomes ........................................................ 131 Restriction Sites .......................................................... 131 EcoRI-De®ned DNA Repeat ............................................... 131 Summary ................................................................ 132 Character Congruence Analysis ............................................... 132 Discussion ................................................................... 135 Comparison of Results of Taxonomic and Character Congruence Analyses ........ 135 Classi®cation of Phyllostomid Bats ........................................... 136 Higher-level Classi®cation ................................................. 136 Generic Considerations .................................................... 140 Interpretation of Chromosomal Data .......................................... 142 Interpretation of Immunological Data ......................................... 145 Uterine Fusion: Progressive and Unidirectional? ................................ 147 Evolution of Facial Features: A Phylogenetic Perspective ........................ 148 Vibrissae ................................................................ 148 The Noseleaf ............................................................ 155 Tracing the Diversi®cation of Feeding Habits .................................. 162 2 2000 WETTERER ET AL.: PHYLOGENY OF PHYLLOSTOMID BATS 3 Summary and Conclusions ..................................................... 170 Acknowledgments ............................................................ 172 References ................................................................... 173 Appendix 1: Specimens Examined .............................................. 184 Appendix 2: Data Matrix ...................................................... 188 Appendix 3: Discrete-State Characters Not Included In This Study ................. 192 Appendix 4: Taxonomic Diagnoses ............................................. 192 4 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY NO. 248 ABSTRACT Phyllostomidae is a large (. 140 species), diverse clade of Neotropical bats. Different species in this family feed on blood, insects, vertebrates, nectar, pollen, and fruits. We inves- tigated phylogenetic relationships among all genera of phyllostomid bats and tested monophyly of several genera (e.g., Micronycteris, Mimon, Artibeus, Vampyressa) using 150 morphologi- cal, karyological, and molecular characters. Results of parsimony analyses of these combined data indicate that all traditionally recognized phyllostomid subfamilies are monophyletic and that most taxa that share feeding specializations form clades. These results largely agree with studies that have used a taxonomic congruence approach to evaluate karyological, immuno- logical, and limited sets of morphological characters, although our ®nding that Phyllostominae is monophyletic is novel. Our results indicate that several genera (Micronycteris, Artibeus, and Vampyressa) are not monophyletic. We propose a new classi®cation for Phyllostomidae that better re¯ects hypothesized evolutionary relationships. Important features of this new classi- ®cation include: (1) formal recognition of two clades that group nectarivorous and frugivorous subfamilies, respectively, (2) rede®nition of Glossophaginae and recognition of two tribal-level taxa within that subfamily, (3) recognition of several tribal-level taxa in Phyllostominae, (4) formal recognition of two clades that have been colloquially referred to as ``short-faced'' and ``long-faced'' stenodermatines, (5) elevation of the subgenera of Micronycteris to generic rank, (6) recognition of Mesophylla as a junior synonym of Ectophylla, (7) recognition of Enchis- thenes as a distinct genus, and (8) retention of Dermanura and Koopmania as subgenera of Artibeus. Although Vampyressa is not monophyletic in our tree, we recommend no nomen- clatural change because we did not include all Vampyressa species in our study. Comparisons of character and taxonomic congruence approaches indicate that character congruence provides improved resolution of relationships among phyllostomids. Many data sets are informative only at limited hierarchical levels or in certain portions of the phyllostomid tree. Although both chromosomal and immunological data provide additional support for sev- eral clades that we identi®ed, these data sets are incongruent with many aspects of our phy- logenetic results. These con¯icts may be due to methodological constraints associated with the use of karyological and immunological data (e.g., problems with assessing homologies and distinguishing primitive from derived traits). Among other observations, we ®nd that Macrotus waterhousii, which has been thought to have the primitive karyotype for the family, nests well within the phyllostomine clade. This suggests that results of previous analyses of chromosomal data may need to be reevaluated. Mapping characters and behaviors on our phylogenetic tree provides a context for evaluating hypotheses of evolution in Phyllostomidae. Although previous studies of uterine evolution in phyllostomids and other mammals have generally supported the unidirectional progressive fusion hypothesis, our results indicate that intermediate stages of external uterine fusion are often derived relative to the fully simplex condition, and that reversals also occur with respect to internal uterine fusion. Uterine fusion therefore appears to be neither completely unidirec- tional nor progressive in Phyllostomidae. Evolution of the vibrissae and noseleaf is similarly complex and homoplasy is common in these structures; however, many transformations in these systems diagnose clades of phyllos- tomids. Within Phyllostomidae, there is considerable derived reduction in numbers of vibrissae present in various vibrissal clusters. The phyllostomid noseleaf seems to have become a much more elaborate and complex structure over evolutionary time. Primitively within the family, the spear was short, the internarial region was ¯at, and the horseshoe was undifferentiated from the upper lip. Subsequently, within the various subfamilies, the spear became more elongate, the central rib and other internarial

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