“3 ...I. . u... d. i . . nvfiaium. n ...».. @va uifi?.fl. E. .3 . .. 4 ‘15.. .. :31 \t. 3:29.71 : .1 . «an... Lia, .«u. k“. :“Jv‘fi. 1!, Ex . .rul‘nm W." fit: «(I «\l‘er.‘ n.4,... yin}. E3: .7 Date This is to certify that the thesis entitled PHYLOGENY OF THE NEOTRPICAL NECTAR-FEEDING BATS (CHIROPTERA: PHYLLOSTOMIDAE) presented by Bryan Charles Carstens has been accepted towards fulfillment of the requirements for Masters degree in Zoology Major professor April 20th, 2001 0-7639 MS U is an Affirmative Action/Equal Opportunity Institution LIBRARY Michlgan State Unlverslty PLACE IN RETURN Box to remove this checkout from your record. To AVOID FINES return on or before date due. MAY BE RECALLED with earlier due date if requested. DATE DUE DATE DUE DATE DUE fill AfL E W U' 9 19 1‘ F 1 0 8/01 cJCIRC/DateDuepBS-DJS PHYLOGENY OF THE N EOTROPICAL NECTAR-FEEDIN G BATS (CHIROPTERA: PHYLLOSTOMIDAE) By Bryan Charles Carstens A THESIS Submitted to Michigan State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Department of Zoology 2001 ABSTRACT PHYLOGENY OF THE NEOTROPICAL NECTAR-FEEDING BATS By Bryan Charles Carstens As pollinators for more than 300 species of plants, the nectar-feeding members of the Phyllostomidae are an important component of neotropical ecosystems. I present a phylogeny of 35 species of nectar-feeding bats based on 119 morphological characters: 62 from the skull and skeleton and 57 soft tissue characters (the later from Wetterer et al. 2000). These data strongly support monophyly of the subfamilies Glossophaginae, Phyllonycterinae, and Brachyphyllinae, as well as the tribes Glossophagini and Lonchophyllini. Analysis of a combined matrix, including both the morphological charac- ters and DNA sequences from the RAG-2 gene (taken from Baker et al., 2000), results in a phylogeny with the same topology as that produced by the morphological data alone. Support for major clades is stronger than in the morphological tree, but support for basal nodes of the phylogeny remains weak. The weak support at these basal nodes underscores the historical disagreements regarding relationships among the subfamilies; combining morphological and molecular data has improved support for these nodes only slightly. Uncertainty regarding basal relationships complicates description of morphological change during the evolution of nectarivory in the Phyllostomidae. The phylogeny I present suggests a progressive reduction of the upper and lower incisors, which has increased the space available at the front of the mouth for the tongue to pass through during feeding. This transition may have opened new feeding niches to glossophagine bats. ACKNOWLEDGEMENTS ‘ I am grateful to the chair of my committee, Dr. Barbara Lundrigan, for encouragement and support that began during my time as an undergraduate. The advice and expertise of . Dr. Philip Myers, Dr. Donald Straney, and Dr. Jeffrey Conner, the other members of my graduate committee, have proved to be invaluable to the completion of this project. I also wish to thank curators and technical assistants at the American Museum of Natural History, the Field Museum of Natural History, the National Museum of Natural History, the Museum of Zoology at the University of Michigan, and the Michigan State University Museum, for their assistance during research visits. Dr. Nancy Simmons, Dr. Larry Heaney, and Dr. Bruce Patterson were kind enough to discuss this project with me during research visits, and these conversations greatly improved this thesis. This project would not have been possible without collections studies grants from the American Museum of Natural History and the Field Museum of Natural History, or specimen loans from the Museum of Zoology at the University of Michigan or the National Museum of Natural History. Finally, I wish to thank my colleagues at the Michigan State University Museum for their friendship and support. 111 TABLE OF CONTENTS List of Tables .......................................................................................... v List of Figures ........................................................................................ vi Introduction ............................................................................................ 1 Methods ................................................................................................ 9 Results ................................................................................................ 34 Discussion ........................................................................................... .39 Appendix I ........................................................................................... 48 Appendix II .......................................................................................... 54 Literature Cited ...................................................................................... 59 iv LIST OF TABLES Table 1: Taxonomic names of nectar-feeding phyllostomid bats ............................... 5 Table 2: Characters most likely to be convergent due to feeding ............................. 32 Table 3: Ingroup sampling completeness for morphological data ............................ 34 LIST OF FIGURES Figure 1: Phylogeny based on the Rag-2 gene .................................................... 8 Figure 2: Three types of uropatagium ............................................................ 10 Figure 3: Ventral view of the premaxillary region .............................................. 11 Figure 4: Character 5 shown with an arrow on Monophyllus plethodon ..................... 1 1 Figure 5: Lateral view of Choeronycteris mexicana ............................................ 12 Figure 6: Incomplete formation of the premaxilla .............................................. 12 Figure 7: Lateral view of Phyllonycteris poeyi .................................................. 13 Figure 8: The basiocranial region of Glossophaga soricina ................................... 13 Figure 9: Ventral view of Choeronycteris mexicana ............................................ 14 Figure 10: Ridge dividing the basioccipital, shown in Lonchophylla thomasi .............. 15 Figure 11: Detail of the presphenoid and bassioccipital region in L0. mordax ............. 16 Figure 12: Crown of Lonchophyllini incisors ................................................... 16 Figure 13: Frontal view of mandible ............................................................. 17 Figure 14: Frontal view of the canines ........................................................... 17 Figure 15: Occlusal view of the rostrum of Lionycteris spurelli, showing the cusp described in character 28 .................................................................. 18 Figure 16: Concave lingual margin of the first premolar of Leptonycteris (right), with Glossophaga shown on left ............................................................... 18 Figure 17: Occlusal view of first lower molar ................................................... 19 Figure 18: Height of metacone and protocone ................................................... 20 vi Figure 19: Anterior view of the pointed upper incisor crowns in Brachyphylla cavemarum ................................................................................. 20 Figure 20: Cingular shelf at posterior base of upper incisors in Brachyphylla spp ........ 20 Figure 21: Frontal view of Choeronycteris mexicana ......................................... 21 Figure 22: Inflected cusps of upper outer incisors in Anoura caudifer ....................... 21 Figure 23: Occlusal View of the last upper premolar ........................................... 23 Figure 24: First upper molar of Glossophaga (left) and Monophyllus, illustrating the hypocone and the parastyle ............................................................... 23 Figure 25: First lower molar of Phyllonycteris poeyi (left) and Lonchophylla robusta, illustrating the absent paraconid in the former .................. ' ....................... 24 Figure 26: Uptumed stylar shelf .................................................................. 25 Figure 27: Leptonycteris yerbabuenae in the lateral view illustrating the height of the metacone .................................................................................... 25 Figure 28: Phylogeny based on morphological data ............................................ 36 Figure 29: The most parsimonious tree. . . .from RAG-2 and Morphological data .......... 39 Figure 30: The frontal gap .......................................................................... 41 Figure 31: Single upper incisors in Choeroniscus minor ....................................... 43 Figure 32: Reduction of zygomatic ................................................................ 46 vii Introduction This paper investigates the evolution of specialized nectarivory in the Phyllostomidae using data from morphology and molecular sources. The Phyllostomidae, a neotropical family with over one hundred and forty species, is distinguished by the wide variety of resources its species exploit. Blood, nectar, pollen, fruit, nuts, seeds, parts of flowers, insects, lizards, birds, mammals, and frogs are eaten by various members of the family. This range of diets has stimulated interest in the evolution of feeding strategies (Gillette, 1975; Ferrarezzi and Gimenez, 1996; Wetterer etal., 2000). A phylogeny for three phyllostomid subfamilies, the Brachyphyllinae, Glossophaginae, and Phyllonycterinae, will be developed and used to investigate the evolution of morphologies associated with specialized nectarivory. Most phyllostomid species show flexibility in the food resources they exploit; this plasticity has also provided opportunities for a switch to nectar feeding. The first phyllostomid bat to ingest nectar probably did so while visiting the flower for other reasons, perhaps to glean insects from the plant or to eat fruit. Many extant phyllostomid species supplement their diet with pollen or nectar in a way that may be similar to the ancestral behavior; these including Rhinophylla pumilio, Anibeus jamaicensis, Vampyrops lineatus, Phyllostomus discolor, Phyllostomus hastatus, Carollia perspicillata, and Sturm'ra lilium (Heithaus et al., 1974; Heithaus et al., 1982; Hopkins, 1984; Ramirez et al., 1984; Buzato and Franco, 1992; Gribel and Hay, 1993; Valiente- Banuet et al., 1997; Gribel et al., 1999). This list includes bats that are primary frugivores and primary insectivores, and while nectarivory in the paleotropical Pteropodidae evolved from frugivory (Kirsch and Lapointe, 1997), there is no reason to assume that the situation was the same in the neotropics. There is also no a priori reason to assume that nectarivory in the Phyllostomidae has evolved only once. The focus of this study is limited to the Glossophaginae, Phyllonycterinae, and Brachyphyllinae. Species in these subfamilies are primarily nectarivorous, but supplement their diet with fruits or insects. The taxa listed in the previous paragraph merely supplement their diets with nectar. One quarter are endemic to islands in the Caribbean; these endemics include six species in the Phyllonycterinae, both species in the Brachyphyllinae, and two species in one glossophagine genera, Monophyllus. The remaining members of the large subfamily Glossophaginae are distributed from northern Mexico to northern Chile and Argentina (Eisenberg and Redford, 2000; Eisenberg and Redford, 1992; Eisenberg, 1989). Several morphological features associated with feeding are common in the nectar- feeding bats of the Phyllostomidae: a long, extensile tongue covered in brush-like papillae, an elongated rostrum, loss or reduction of the incisors, reduction of the molars and premolars, reduction of the noseleaf, and an overall trend towards a smaller body size and lower mass. These morphological characters compose the primary differences in morphology between the nectar-feeding subfamilies and the members of the Phyllostomidae that utilize other food resources. There are also significant differences in behavior between hats that feed opportunistically on pollen or nectar and those that feed primary on pollen and nectar. Opportunistic nectar feeders such as Phyllostomus discolor land on a plant and feed at a flower while hanging onto the stem with their hind legs (Heithaus et al., 1982; Gibbs et al., 1999). Glossophagine bats hover in front of the flower and feed in a manner similar to hummingbirds, sticking their face into the corolla and using their tongue to lap up nectar and pollen. Hovering flight is energetically expensive and may place a constraint on the size of the bats. Even the smallest glossophagine bats usually hover for fewer than two seconds at a time (Winter, 1998; Winter and Helverson, 1998; Voight and Winter, 1999). Glossophagine bats forage individually, feeding in what has been described as a trap~line manner—moving from one plant to the next, drinking small quantities of nectar at each stop (Heithaus et al., 1974; Voss et al., 1980; Gibbs et al., 1999; Machado et al., 1998). Opportunistic feeders, in contrast, tend to forage in groups and can drain the entire corolla of nectar before moving on (Heithaus et al., 1974; Fisher, 1992). These behavioral differences underscore what is to the plant the most significant difference between glossophagines and opportunistic nectar feeders, that the glossophagine bats are more effective as pollinators (Heithaus et al., 1982; Herrera and Del Rio, 1998). These pollination services have allowed the Glossophaginae to influence the size, shape, density, and nectar concentrations of their host plants (Hopkins, 1984; Eguiarte and Burquez, 1987; Gribel and Hay, 1993; Luckow and Hopkins, 1994). In turn, the evolution of structures involved with feeding in nectarivorous bats has been influenced by the morphology of the flowers of their host plants. While characteristics such as the elongated rostrum, reduction of incisors, and extensible tongue can be easily imagined as adaptations for nectar feeding, few (if any) glossophagines are limited to nectar as a resource. Most are generalist feeders that are capable of consuming insects and fruit in addition to nectar, a characteristic that could be an important survival strategy to cope with fluctuating nectar supplies. The percentage of nectar in the diet of glossophagine bats also exhibits seasonal, interpopulational, and intrapopulational variation (Fleming et al., 1972; Heithaus et al., 1975; Sazima, 1976; Fleming and Heithaus, 1986). If ancestral phyllostomid bats were similar to their modern descendents in the breadth of their diet, it is likely that there was ample opportunity for populations to evolve towards specialized nectarivory. A phylogeny that is robust and well supported would allow a more informed inferences on the number of times primary nectarivory has evolved. The taxonomic history of the nectar-feeding phyllostomid bats has been dominated by questions pertaining to the relationships of four major groups; Brachyphyllinae, Phyllonycterinae, Glossphagini, and Lonchophyllini (Table 1). The earliest classifications of this group included Brachyphylla with the stenodermatines and classified the remaining nectar feeders as the Glossophagae (Dobson, 1875). Shortly thereafter, the Phyllonycterinae was elevated to subfamily status (Miller, 1907). The separation of Brachyphylla from the Phyllonycterinae was maintained by subsequent revisions (Simpson, 1945; de le Torre, 1961; Koopman and Jones, 1970), until Silva- Taboda and Pine (1969) used arguments from morphology and behavioral observations to include Brachyphylla as a member of the Phyllonycterinae. There has been little consensus over the last thirty years about the relationship between Brachyphylla, Phyllonycterinae, and Glossophaginae; some works have included Brachyphylla in the subfamily Phyllonycterinae (Smith, 1976; Corbet and Hill, 1980; Baker et al. 1981), some have elevated Brachyphylla to a monotypic subfamily (Griffiths, 1982; Griffiths, 1983; Gimenez, 1996; Wetterer et al., 2000), and others have argued that Brachyphylla and the Phyllonycterinae form a clade within the Glossophaginae (Gardner, 1977; Baker and Bass,1979; Honeycutt and Sarich, 1987, McKenna and Bell, 1997). One paper Table 1: Taxonomic names of nectar-feeding phyllostomid bats examined here (after Wetterer, et al., 2000). Sub-family "It'ibe Genera Species Brachyphyllinae Brachyphylla cavernarum nana Phyllonycterinae Phyllonycteris aphylla poeyi Erophylla bombifrons sezekorni Glossophaginae Glossophagini Anoura * caudifer cultrata geoflroyi Iatidens Choeronycteris“ maxicana Choeroniscus“ godmani minor periosus Hylonycteris“ underwoodi Lichonycteris“ obscura Musonycteris“ harrisom' Scleronycteris" ega Glossophaga commissarisi Ieachii longirostris morenoi soricina Leptonycteris curasoae nivalis yerbabuenae Monophyllus plethodon redmani Lonchophyllini Lionycteris spurelli Lonchophylla handleyi hesperia mordax robusta thomasi Platalina genovensium *Indicates genera without lower incisors. reduced the Glossophaginae (including Lonchophylla, Lionycteris, Brachyphylla, and Phyllonycteris) to tribal status within the Phyllostominae (Baker et al., 1989), and molecular data suggest that none of these classifications reflect the history of this group (Baker et al., 2000). Hypotheses about relationships within the Glossophaginae have been just as contentious as the higher level relationships. Numerous authors have suggested that Glossophaginae is not monophyletic. In 1967, Baker proposed that Glossophaginae is "an artificial grouping of species evolving to a nectar feeding way of life from two or more independent lines." He supported this proposal with data from chromosomes and analysis of immunological reactions of blood sera (Baker, 1967). Phillips (1971), using characters from the dentition, found evidence for two separate clades of glossophagines. Gardner (1977) used chromosomal data to propose three main clades of nectar-feeding phyllostomid bats. Numerous phylogenies derived from different sources of data have been published, but there is little agreement among them (Baker et al., 1981; Haiduk and Baker, 1982; Griffiths, 1982; Van Den Bussche, 1991; Van Den Bussche, 1992, Gimenez et al., 1996; Baker et al., 2000). That different sources of data result in different phylogenies for the same species is not surprising. There is no a priori reason to prefer, for example, a tree derived from dental characters to one derived from nuclear DNA. The best hypothesis of the relationship of these species should come from a combination of all available data (Kluge, 1998). Wetterer et al., (2000) combined skull and soft tissue morphology, the sex-determination system, and rDNA restriction site data to derive a phylogeny for genera of the Phyllostomidae. This tree suggests that the Glossophaginae is monophyletic, that Phyllonycterinae is the sister taxon to Glossophaginae, and that Brachyphylla is basal to this group and a large clade containing all of the remaining phyllostomid bats (with the exception of the Desmodontinae). The first molecular study to investigate relationships in the entire family is by Baker et al., (2000), who published a phylogeny (Fig. 1) from the nuclear Recombination-Activating Gene-2 that has significant points of disagreement with Wetterer et al., (2000). These concern the relationship of the major clades. The molecular data argue for a monophyletic clade composed of Brachyphyllinae, Phyllonycterinae, and three genera of glossophagine bats (Leptonycteris, Glossophaga, and Monophyllus), with the clade of the most specialized nectar feeders (Anoura, Musonycteris, Choeroniscus, C hoeronycteris, and Hylonycteris) sister to it The clade composed of Lonchophylla and Lionycteris is sister to Lonchorhina, an insectivorous member of the subfamily Phyllostominae. The molecular data suggest that primary nectarivory evolved independently in the Lonchophyllini and the clade formed by Glossophagini + Phyllonycterinae + Brachyphylla. In this study, I add characters from the cranium and dentition to data from Wetterer et al. (2000), in order to generate a morphological phylogeny for the nectar feeding bats of the Phyllostomidae. I then combine these data with the sequence data from Baker et a1. (2000), and identify a single most parsimonious tree from all available data. This phylogeny is used to investigate the evolutionary morphological features associated with specialized nectarivory, such as the elongated rostrum and the reduced dentition. Ametrida , _L5_6':Sphaemnycteris 57 Centurio Pygoderma J—-A rdops 85 66 87 62 88 98 98 9 9j—A riteus Stenoderrna Artibeus hirsums WEArtibeus concolor 96 L——Dermanura E nchisthenes Ectophylla C hiroderma ‘ Mesophylla . a: Vampyressa pusr'lla Platyrrhinus 78 Y4: Vampyrodes ._ Uroderma Vampyressa bidens Sturnira Rhinophylla Carollia 76 Glyphonycteris daviesi fi Dinyctert's 97 Glyphonycteris sylvesm's mcLonchophylla Lonchophyllini Lionyctert's Lonchorhina Anoura ——Musonycteris Glossophagini 99 —gzoemm'scus_ without lower __ oeronycterts - - 100 Hylonycteris incisors , Brachyphylla Brachyphyllmale I—Erophylla 99 l—Phyllonycteris Phyllonycterinae Glossophagini with lower incisors Leptonycteris , _[6EE Glossophaga 82 Monophyllus Vampyrum g: C hrotopterus ——Mimon 68 —Phylloderma 93 l—Phyllostomus Tonatt‘a l'_ flachops firoup Out 61 l—Il«!acrophyilum Desmodus mEDiamus 77 L—Diphylla Lampronycteris Micronycteris schmidtorum 7 7 ‘ 00 Micronyctert's minuta 99 Micronycteris hirsuta TICMicmnycteris megalotis r—Macrotus waterhousii IOOLMacmtw californicus Figure 1: Phylogeny based on the RAG-2 gene. The phylogeny of the Phyllostomidae, from Baker, et al., (2000). Tree length=1122 steps, Consistency index=0.4180, and Rentention index=0.6643. Numbers below the braches are bootstraps from 200 iterations. 8 Methods I collected character data from the skulls of representatives of 35 species of phyllostomid nectar-feeding bats. Specimens (674 total) were examined at the American Museum of Natural History, the Field Museum of Natural History, the Michigan State University Museum, the Museum of Zoology at the University of Michigan, and the National Museum of Natural History (Appendix I). I assumed monophyly of the Phyllostomidae, and five phyllostomid species (Macrotus califomicus, Carollia perspecillata, Artibeus jamaicensis, Phyllostomus discolor, and Desmodus rotundus) and one morrnoopid (Pteronotus pamelli) were used as outgroups. These species were chosen as outgroups based on their relationships to the nectar-feeding phyllostomid bats in recent publications (Simmons, 1998; Simmons and Geisler, 1998; Wetterer et al., 2000; Baker et al., 2000). Due to the high degree of character variability within certain genera, species were used as terminal taxa. With the exception of Lonchophylla and Phyllonycteris, all recog- nized species were sampled from each genera (Novak, 1994; Wilson and Reader, 1993). Three species from Lonchophylla (L. dekeyseri, L. concava, and L. bokermam') and two from Phyllonycteris (P. major and P. obtusa) were not available to me. Sixty-two characters from the skull and dentition of the nectar-feeding phyllostomid bats were coded. All characters were evaluated following the criteria listed below: a) Characters are identifiable across all taxa. b) Most characters are binary with ‘0’: absent; ‘1 ’=present. In some cases, addi- tional character states (2, 3, 4) are used to designate alternative forms of a character. c) All characters are unordered. d) All characters are equally weighted. e) Characters that are polymorphic within a species are recorded in the data matrix as having both character states. f) Sampling is repeatable in examinations at different times and museums. Inconsis- tent characters are considered too ambiguous to use. g) Taxa that are missing an anatomical feature on which another character is based are coded with a ‘-’ in the data matrix. For example, taxa without lower incisors were coded as a ‘-’ on characters that concern the crown of the lower incisor. This was done to avoid an artificial weighting of these missing characters. h) Characters are coded in a reductive manner (Wilkinson, 1995). Characters 13, 22, 24, 25, 26, 28, 31, 41, 42, 45, 46, 50, 58, and 61 are based on descriptions found in Phillips (1971). 1. Condition of Uropatagium. Uropatagium unreduced, extending to or past the level of the foot (0); or to level of the knee (1); or greatly reduced (2). The uropatagium of most nectar-feeding phyllostomid bats is reduced in size compared to that of many other members of the family (Fig. 2). Bats such as Anoura geofiroyi either lack a calcar or have a calcar that is reflected to run parallel to the tibia; the uropatagium of these species is reduced and closely follows the hind legs (2). The uropatagium of most glossophagines, such as Lonchophylla thomasi, is complete to or below the level of the knees, giving it the appearance of having a “u” shape removed (1). These bats usually have a well developed calcar (see charac- ter number 2), “mic" is perpendicu- Figure 2: Three types of uropatagium. From left to right, the drawings correspond to character lar to the tibia and supports the distal states ‘0’ . 1’ and ‘2’ from character 1, end of the patagium in a manner similar to other phyllostomid bats. Unreduced uropatagia extend to the feet or beyond, as in Macrotus californicus (O). 2. Presence of calcar (Straney, 1980; Wetterer et al., 2000). The calcar, a spur of cartilage or bone that projects from the ankle and supports the ur0patagium, is equal to or longer than the length of the foot in most phyllostomid bats (0). In most nectar-feeding bats a calcar is present, but it is shorter than the length of the foot (1 ). Exceptions include 10 Phyllonycteris spp. and Brachyphylla spp., in which the only evidence of a calcar is a Small bony protrusion on the ankle (2), possibly homologous with a true calcar. 3. Tail length (Straney, 1980; Wetterer et al., 2000). The tails of most glossophagines are short and enclosed in the uropatagium (0). In Macrotus, the tail extends past the length of the hind legs (1). In other nectar-feedering phyllostomid bats (most Anoura and Leptonycteris) no tail is visible (2). 4. Premaxillary region with three foramina (Fig. 3). Three major foramina character— ize the premaxillary region of the cranium in most members of the Glossophaginae (1). These are ori- ented in a triangle, with the most anterior foramen just posterior to the upper incisors. However Lichonycteris obscura, Lionycteris spurelli, and Scleronycteris ega ~ Figure 3: Ventral view of the all lack the most anterior foramen, as do the premaxillary region. The three foramina characteristic Brachyphyllinae and Phyllonycterinae (0). This of glossophagine bats are shown (character 4). appears to be the ancestral condition for the Phyllostomidae, as all members of the outgroup have two foramina in their premaxilla. 5. Foramen between the foramen ovale and mandibular fossa. Several foramina are found at the base of the skull of phyllostomid bats. All nectar-feeding bats have a large foramen, the foramen ovale, on either side of the palatine. A smaller foramen is sometimes found posterior to it, between the anterior portion of the pterygoid and the mandibular fossa (1). Several Figure 4: Character 5 shown with an arrow on Monophyllus plethodon. taxa lack this foramen (0)' 6. Foramen at the anterior ' margin of the orbital region (Fig. 5). While nectar feeding phyllostomid bats lack an orbital Figure 5: Lateral view of Choeronycteris mexicana. The arrow marks the location of the process. two taxa (Choeronycter is foramen describen in character 6. mexicana and Musonycteris harrisoni) have a foramen in the approximate place where the orbital process occurs in other bats (1). Other taxa sampled lacked this foramen (0). 7. Foramen between the interior incisors (Fig. 6). In most bats with three foramina in their premaxillary region (character 4), the most anterior foramen is located posterior to the first upper incisors (O). In some species of the genera Anoura and Choeroniscus, the most anterior foramen is located between the inner incisors (1). This character is some- times polymorphic within species, as some specimens of Anoura spp. and Choeroniscus spp. that lack this foramen have a ‘v'- . 0 . . shaped indentation in the premaxilla. This is interpreted to be an incomplete Figure 6: Incomplete formation of the pre- formation of the premaxilla as a result maxilla. Diagram of the premaxillary region showing the polymorphism in some species of Anoura and Choeroniscus for character 7. coded (1). of this most anterior foramen, and 8. Anterior projection of lower portion of the mandible. The mandible of some glossophagines, such as Lichonycteris obscura, have a bony protrusion extending anteriorly and ventrally from the lateral view, so the the most anterior portion of the dentary approaches the ventral margin of the dentary (1). Most species lack a projection and the most anterior point of the dentary is the medial portion (0). 9. Lateral compression of region separating the anterior portion of the pterygoids from the rostrum (Fig. 7). The dorsal region between the anterior portion of the ptery- goids and the posterior portion of the palatine is laterally compressed in members of the genus Phyllonycteris, which results a slight separation of this region from the sphenoid region (1). Other phyllostomid bats lack this separation (0). 10. Presphenoid ridge (Fig. 8). Many nectar feeders have a longitudinal ridge along the midline of the presphenoid region (1). The presphenoid ridge is lacking in some genera, including Anoura and Choeroniscus (0). Much like the basioccipital in character 16, the presphenoid region has a slightly thickened medial portion that can appear ridge-like, but clearly differs from the well developed ridge of Figure 8: The basiocranial taxa like Glossophaga soricina. 11. Pterygoid alae (Alvarez et. al., 1991) (Fig. the pterygoid alae with a ‘B‘, 8). The posterior part of the pterygoid of of the spenoid region with a Glossophaga soricina and Glossophaga leachii has 1 l, and 14, respectively. Figure 7: Lateral view of Phyllonycteris poeyi. The arrow points to the region described in character 9. region of Glossophaga soricina. The presphenoid ridge is marked with an ‘A’, and the protrusion at the base ‘C’; illustrating characterle, small projections (alae) that protrude towards the auditory bullae ( 1). Other phyllostomid bats lack these protrusions on their pterygoids (0). 12. Peninsular fusion of the posterior edge of the palatine bone. The palatine region of most nectar feeding bats is fused in such a manner that the anterior point along the posterior margin of the palatine is smooth, giving the entire posterior margin the appear- ance of a smooth arc (0). In the genus Anoura the posterior margin of the palatine is interrupted by a small peninsula of bone that forms along the medial axis of the palatine region and projects posteriorly between the pterygoids (1). 13. Inflated posterior tip of pterygoid (Wettereret al., 2000) (Fig. 9). The posterior tip of each pterygoid is enlarged while the base is expanded and curves inward, bringing the tip nearly into contact with the ante- rior margin of the auditory bullae in Choerom'scus spp., Choeronycteris mexicana, and Musonycteris harrisom' (l). The pterygoid tips of other nectar feeders are not inflated (0). 14. Protrusion at medial posterior margin of sphenoid region (Fig. 8). A bony process at the base 0f the sphen01d Figure 9: Ventral view of C hoeronycteris mexicana. The arrow marks the inflated tip of the pterygoid (character 13). The posterior margin of the sphenoid hangs over the basioccipital region in C. mexicana (character 15) just above the ‘A’ on either side of the ridge dividing the occipital. region projects over the anterior portion of the occipital bone in several taxa, including Glossophaga soricina (1). Most species lack this process (0). 15. Overhanging posterior margin of the sphenoid (Fig. 9). The posterior portion of the sphenoid region extends over anterior portion of the basioccipital in Choeronycteris mexicana and Musonycteris harrisom', creating two small pockets on either side of the medial ridge dividing the basioccipital (l). The posterior margin of the sphenoid in other phyllostomid bats, while it may be elevated above the basioccipital, does not extend past Figure 10: Ridge dividing the anterior portion of the basioccipital (0). the basioccipital, shown in Lonchophylla thomasi. l6. Ridge dividing the basioccipital. A prominent ridge that is narrow and significantly elevated above the level of the basioccipital divides the basioccipital along its medial axis in many taxa, including Lonchophylla thomasi (1 ). This is distinguished from the slightly thickened medial portion of the basioccipital in most phyllostomid by both the difference in elevation and the width. Taxa without a prominent ridge are coded (0). 17. Zygomatic arch (Lim,l993). Most phyllostomid bats have a complete zygomatic arch (l). The arch is incomplete in nectar feeders, including Choeroniscus spp. and Lonchophylla spp. (0). When present it is reduced in robustness. All taxa with a complete zygomatic are coded (1), regardless of the relative thickness of the arch. 18. Sagittal crest. The sagittal crest is absent in all members of the Glossophaginae and Phyllonycterinae (0). A sagittal crest is present in most other phyllostomid bats, including the Brachyphyllinae (l). l9. Horiontal plane of the presphe- noid and basioccipital equal. In the Lonchophyllini, the basioccipital is on the same horizontal plane as the presphenoid . (1). In other glossophagines and the outgroup, the presphenoid is ventral to the basioccipital when seen in the lateral View (0). Figure 11: Detail of presphenoid and basioccipital region in Lonchophylla 20. Median gap between lower mordax. The horizontal plane of these regions are approximately equal. incisors. Some taxa that have retained the lower incisors have a median gap be- tween the inner incisors (1). Other taxa with lower incisors lack this gap (0). 21. Number of lower incisors (Wetterer et al., 2000). The reduction in number of lower incisors is one of the most noticeable characteristics of the glossophagine jaw. Freeman (1995) considered this to be the result of selection for the unhindered movement of the tongue during feeding. Most phyllostomid bats have two lower incisors (2), but many species of glossophagines are missing the lower incisors entirely (0). 22. Trifid crown on lower incisors (Fig. 12). The Lonchophyllini possess a trifid O crown on their lower incisors (1). On these " ’ Figure 12: Crown of incisors in the teeth two vertical grooves d1v1de the crown Lonchophyllini. The trifid crown on the lower incisor (character 22), seen in the frontal (left) and occlusal (right) vrews. phyllos tomi d bats lack the trifi d crown (0). of the tooth into three lobes. Other 16 23. The lower incisor crowns form a shallow ‘u’ shaped depression in the frontal view (Fig. 13). Some genera, such as Erophylla spp., have first incisors Figure 13: Frontal View of the mandible. Incisors with their crowns in a shallow ‘u’- with crowns that are lower in elevation shaped depression (right) and with crowns level (left) are shown. than the crowns of the outside incisors, a pattern that results in a shallow ‘u’-shaped incisor row in frontal view( 1 ). Other genera, such as Lonchophylla, have incisors with crowns that are level (0). 24. Curved canines (Fig. 14). The canines of most glossophagine bats appear to be bowed outward, giving them a curved appearance in the frontal view (1). Lichonycteris obscura and Scleronycteris ega are exceptions with straight lower canines (0). Most Figure 14: Frontal view of canines. Straight (left) and curved (right) are shown. other phyllostomid bats, including the Brachyphyllinae and Phyllonycterinae, also have straight lower canines. 25. Anterior lingual Cingular shelf on lower canine. The lower canines have an anterior lingual Cingular shelf that articulates with the shearing surface of the outer upper incisors in Glossophaga, Leptonycteris, and Lonchophyllini (1). This Cingular shelf is absent in other nectar-feeding phyllostomid bats (0). 26. Posterior lingual Cingular shelf. The lower canines of most phyllostomid nectar feeders have a posterior lingual shelf that occludes with the anterior Cingular shelf of the upper canine (1). Species that lack this shelf include members of the genera Anoura and Choeroniscus (0). 27. Number of lower premolars. All members of the Glossophaginae have three lower premolars (3). Other nectar feeders have two (2). 17 28. Elongated labial cusp on the second lower premolar (Fig. 15). Lionycteris spurelli and Brachyphylla spp. have a ' large labial cusp on the second lower premolar that extends to over half of the height of the lower canine (1). Other nectar-feeding phyllostomid bats lack an elongated labial cusp on the last lower premolar (0). 29. The three cusps on the lower premolars approxi- mately equal in height. The three cusps on each lower premolar are at approximately the same elevation in Choeroniscus spp. (1). Other glossophagines have premolars in which the middle cusp is significantly higher than the other two (0). 30. Width of lower premolars. The width of the lower premolars is approximately equal to the width of the lower molars in most glossophagines (0). In species with an Figure 153 Occlusal view of the rostrum of . elongated rostrum, the lower Lioncyle’is spurelli, Anterior showing the cusp de— premolars are narrower than the scribed in character 28. Lingua lower molars (l). 31. First premolar has a concave lingual margin (Fig. 16). A concave lingual margin on the first premolar in Leptonycteris Figure 16: Concave lingual margin of first premolar of Leptonycteris (right), with Glossophaga shown on left. spp. appears to be formed by a labial migration of the medial portion of the tooth (1). Other taxa have no lingual curve to the first premolar (0). 32. Number of lower molars. Leptonycteris spp. and Lichonycteris obscura have two lower molars (2), while other nectar-feeding phyllostomid bats have three (3). 33. Parallel raised cristid ridges on first lower molar (Fig. 17). The talonid of the first lower molar of Lonchophylla spp. and Lionycteris spurelli has parallel raised cristid ridges that occlude with the protocone on the first upper molar (1). Other phyllostomid bats lack these ridges (0). . 34. Metaconid on first lower molar. The Phyllonycterinae lack a metaconid on the first lower molar (1). The metaconid is present on members of the Glossophaginae and Brachyphyllinae (0). C Anterior Lingual Figure 17: Occlusal view of the first lower molar. The parallel raised cristid ridges (character 33, marked with an ‘A’), the concave lingual margin of the trigondid (char- acter 35, marked with a ‘B’), and the anterior Cingular shelf (character 37, marked with a ‘C’), and are shown. 35. Lingual margin of trigonid on the first lower molar concave (Fig. 17). The lingual margin of the trigonid on the first lower molar is concave in species such as Glossophaga soricina, which gives the anterior half of the first lower molar the shape of a quarter moon (1). The trigonid is ovoid and the interior margin is not concave in other taxa (0). 36. Gap between first and second lower molars. The lower molars have significant gaps between them in many nectar-feeding bats, such as Choeroniscus inca (1). Other nectar-feeding bats lack this gap; their molars are more or less in contact (0). 19 37. Anterior Cingular shelf on trigonid second lower molar has an anterior Cingular shelf on the ' trigonid in Lonchophylla spp. and Lionycteris spurelli (1). Other nectar-feeding phyllostomid bats lack this anterior Cingular shelf (0). 38. Height of protocone and metacone protocone and metacone are much heigher than the rest of the molar in Choeronycteris mexicana and Musonycteris harrisom' (1). The metacone and protocone far beyond the height of the molar in other nectar-feeding (Fig. 17). The Figure 18: Height of metacone and proto- cone. Lateral views of Lionycteris spurelli (above) and Choeronycteris mexicana, the later showing the elevated protocone and meta- cone. (Fig. 18). The are not elevated phyllostomid bats (0). This character may be obscurred in specimens with extremely worn molars. 39. Pointed upper incisor crowns (Fig. Figure 19: Anterior view of the pointed upper incisor crowns ‘ in Brachyphylla cavemarum. same from any point on the incisor crown (0). 40. Cingular shelf at posterior base of the upper incisors (Fig. 20). A Cingular shelf is present at the lingual base of the upper incisors in Brachyphylla spp. Figure 20: Cingular shelf at (1). Other taxa lack this structure (0). 19). The crowns of the first upper incisors are pointed in Brachyphylla spp. (1). The upper incisors of other nectar—feeding bats have crowns that are not pointed; i.e. the distance from any part of the crown to the insertion into the premaxilla is approximately the AnterioT posterior base of upper incisors in Brachyphylla spp. 20 41. Median gap between upper inner incisors (Fig. 21). A medial gap is located between the upper incisors in most of the species that have lost the lower incisors (1). It appears to be Figure 21: Frontal view of Cheoryonycteris mexicana. The median gap between the upper incisors (character 41) is shown. formed by a lateral migration of the upper inci- sors towards the canines. Only Lichonycteris obscura has lost the lower incisors without having a gap between the upper incisors. Two species, Leptonycteris nivalis and Monophyllus redmani, have a gap between the upper incisors, but have not lost the lower incisors. Other species do not have a gap between their upper incisors (O). 42. Spatulate upper inner incisors. Spatulate incisors are flattened and expanded in the distal half of the tooth. Some members of the Lonchophyllini, such as Platalina genovensium and Lonchophylla mordax, have Spatulate upper inner incisors (1), while other nectarivores have small, peg-like upper incisors (0). 43. Inflected cusps of upper outer incisors (Fig. 22). The cusps of the outer upper incisors are not in the same plane as the crown of the inner incisors, but are inflected so Figure 22: Inflected cusps of upper outer incisors in that the height of the crowns decreases on an angle from the Anoura caudifer. crowns of the inner incisors to the gum line (1). Other species lack this inflection in their upper outer incisors, with level crowns in the same plane as the interior incisors (0). 44. Upper inner incisors twice the height of the outer incisors (Wetterer et al., 2000). The upper inner incisors are more than twice the height of the outer incisors in 21 Brachyphylla and Lonchophyllini (1). The Glossophagini all have upper incisors of roughly the same height (0). 45. Long ridge or groove on anterior face of canine. A longitudinal groove runs from near the tip of the canine to its base on the anterior face in Monophyllus plethodon and other taxa (1). This should not be confused with the considerable wear sometimes found on the surface face of canines in many glossophagines, although dental wear sometimes makes identifying this groove difficult. Species that lack the groove are coded (0). 46. Cingulum at anterior base of upper canine. A cingular shelf is present at the anterior base of the upper canine in many nectar-feeding bats (1). Other species lack this structure (0). While some species like Glossophaga longirosm's have three cingular shelves present on the upper and lower canines (described in characters 25, 26, and 46), in Brachyphyllinae, Phyllonycterinae, and Monophyllus spp. there are only two cingular shelves: an upper anterior and a lower posterior (characters 25 and 46). 47. Number of upper premolars. Most nectar-feeding phyllostomid bats have two upper premolars (2). The exception is Anoura, with three (3). 48. Tall cusps on second upper premolar. The cusps on the second upper premolar reach nearly the same height as the tips of the canines in Brachyphylla (1).A11 other nectar feeding phyllostomid bats have upper premolar cusps that are much lower than the canines (0). 49. Cusps of equal height on last upper premolar. In glossophagines like Anoura latidens, the three cusps on the last upper premolar are of approximately the same height (1). Other glossophagines have premolars with a middle cusp that is significantly higher than the two outer cusps (0). 22 50. The last upper premolar has an expanded posterior cingular shelf (Fig. 23). On Glossophaga, Anoura, and Leptonycteris, an expanded posterior cingular shelf charac- terizes the labial margin of the last upper Figure 23: Occlusal views of the last upper premolar. Glossophaga (left) and Lonchophylla (right), illustrating the posterior cingular shelf (character 50). premolar (1). Lonchophylla also has an expanded posterior cingular shelf on the last premolar, but unlike its condition in Glossophaga, Anoura, and Leptonycteris, its base runs from the labial edge to lingual margin of the tooth and is overlapped by the anterior portion of the trigon of the first molar (2). Many of the glossophagines with longer rostra lack a posterior base on the last upper premolar (O). 51. Third and fourth upper premolars in contact ( Lim, 1993; Wetterer et al., 2000). A space is present between the upper premolars in most glossophagines (l). The premolars are always in contact in Brachyphylla and other phyllostomids (O). 52. Number of upper molars. Most members of the Glossophaginae have three upper molars (3). Leptonycteris, Lichonycteris, and some Brachyphylla nana have two (2). 53. Hypocone on first upper molar (Wetterer et al., 2000) (Fig. 24). The hypocone is absent on Figure 24: First upper molar of Monophyllus (left) and the first upper molar in most nectar-feeding Glossophaga, illustrating the hypocone (character 53, with an ‘A’), and the parastyle (character . . _ 54, with a ‘3’) hypocone 18 present, but not in contact With the phyllostomid bats (1). In Monophyllus, the 23 metacone; it slopes toward the palate (2). Other phyllostomid bats have a hypocone and a hypoconal basin (0). 54. Parastyle on first upper molar (Fig. 24). The parastyle on the first upper molar extends in a anterior and labial orientation in Glossophaga soricina and Lionycteris spurelli (1). The parastyle is absent in many taxa which have teeth similar in other respects to taxa with the parastyle (0). 55. Paraconid absent on first lower molar (Wetterer et al., 2000) (Fig. 25). The paraconid is absent on the first lower molar in Brachyphyllinae and Phyllonycterinae (l). The paraconid is present in other taxa sampled here (0). 56. Labial shift in peak of paracone and metacone of the first upper molar. The peaks of the paracone and Figure 25: First lower molar metacone are shifted labially in Brachyphyllinae and of Phyllonycteris poeyi (left) and Lonchophylla robusta, illustrating the absent paraconid in the former. Platalina genovensium, so that the greatest height of these structures is reached near the lingual margin. Other nectar-feeding bats have the greatest height of the para- cone and metacone in the medial region of the molar, resulting in a wide occlusal surface between the lingual margin of the molar and the peak of the metacone or paracone (e. g. Glossophaga soricina and Lonchophylla thomasi) (0). 57. Entoconid on first lower molar (Wetterer et al., 2000). The entoconid is absent on the first lower molar in the Phyllonycterinae (1). Other nectar-feeding phyllostomids have an entoconid on this molar (0). 24 Anterior Labial Figure 26: Uptumed stylar shelf. Located along the labial margin of the first upper molar in the Lonchophyllini, the stylar shelf reaches nearly the same height as the paracone and metacone. 58. Uptumed stylar shelf (Fig. 26). The labial margin of the stylar shelf is upturned, and is nearly as high as the paracone and the metacone on the first upper molar, in the Lonchophyllini and the Brachyphyllinae (1). The Glossophagini and Phyllonycterinae lack an upturned shelf (0). 59. W-shaped ectoloph on the first upper molar (Wetterer et al., 2000). Most insectivorous bats have a ‘w’-shaped ectoloph on their first upper molar, suggest- ing that this is the ancestral condition (1). Other taxa lack the ectoloph, including taxa with an elongated rostrum such as Musonycteris harrisoni (0). 60. Metacone higher than paracone (Fig. 27). The metacone is higher than the paracone on the first upper molar in Leptonycteris (1). In all other nectar feeding phyllostomid bats, the paracone is at least as tall as the metacone (O). Taxa without clearly visible Figure 27: Leptonycteris cusps, such as Erophylla, were coded (0). yerbabuenae in the lateral view illustrating 61. Protocone ridge-like. In the Lonchophyllini and the height 0f metacone. Brachyphyllinae, the protocone on the first upper molar is a ridge-like cusp. This ridge extends along the lingual margin of the tooth and on the anterior edge inflects labially (1). Members of the Glossophagini and the Phyllonycterinae lack a ridge-like protocone (0). 62. Prominent mesostyle. The mesostyle is a relatively large and prominent cusp on 25 the upper molars of bats in the genera Anoura, Lionycteris, and Lonchophylla (1). Other nectar-feeding phyllostomid bats lack a prominent mesostyle (0). In addition to these 62 characters of the skull and dentition, I used 57 soft tissue characters from Wetterer et al. ( 2000). These characters were take directly from their publication and were not re-scored. The following titles of character descriptions are taken directly from their publication The number in the parentheses represents the num- ber used by Wetterer et al., in the original publication. 63. (Wetterer et al., (2000) 84) Third metacarpal longer than fourth or fifth (0); or third and fourth metacarpals subequal in length, both longer than fifth (1); or fourth metacarpal longest (2); or fifth metacarpal longest (4); or third and fifth metacarpals subequal in length, both longer than fourth (5); or third, fourth, and fifth metacarpals all subequal in length (6). 64. (Wetterer et al., (2000) 85) First phalanx of digit III of wing shorter than second phalanx (O); or first and second subequal (l). 65. (Wetterer et al., (2000) 86) First phalanx of digit IV of wing shorter than second phalanx (O); or subequal to second phalanx (1); or longer than second phalanx (2). 66. (Wetterer et al., (2000) 90) M. mylohyoideus undivided (0); or partly divided into anterior and posterior parts by a fleshy aponeurosis (1); or with a pronounced break, clearly divided into distinct anterior and posterior parts (2). 67. (Wetterer etal., (2000) 91) Medial fibers of m. stemohyoideus originate from medial manubrium (0); or from mesostemum (1); or from xiphoid process of sternum (2). 68. (Wetterer et al., (2000) 92) Lateral fibers of m. stemohyoideus originate from manubrium (0); or originate from manubrium and clavicle (l); or originate from clavicle and first rib (2); or originate from xiphoid process (3). 69. (Wetterer et al., (2000) 93) M. stemohyoideus inserts via tendon on basihyal (O); 26 or via raphe into the fibers of m. hyoglossus and m. genioglossus (1). 70. (Wetterer et al., (2000) 94) Part of m. ceratohyoideus inserts on ceratohyal (0); or m. ceratohyoideus does not insert on ceratohyal (1). 71. (Wetterer et al., (2000) 95) M. ceratohyoideus does not insert on stylohyal (0); or part of m. ceratohyoideus inserts on stylohyal (l). 72. (Wetterer et al., (2000) 96) M. hyoglossus originates via tendon from basihyal bone (0); or from raphe which forms insertion of m. stemohyoideus (1). 73. (Wetterer et al., (2000) 97) M. geniohyoideus has single insertion via tendon to basihyal or basihyal raphe (O); or muscle splits near insert directly on anterior surface of basihyal, superficial fibers insert in association with m. hyoglossus and m. stemohyoideus ( 1). 74. (Wettereret al., (2000) 98) Superficial fibers of m. geniohyoideus pass ventral to basihyal and insert into fibers of m. hyoglossus and m. stemohyoideus via raphe (0); or superficial fibers insert in well-developed loop around ventral and dorsal surfaces of the intersection of m. hyoglossus and m. stemohyoideus (l). 75. (Wetterer et al., (2000) 99) Right and left m. geniohyoideus muscles partly or completely fused across midline (0); or muscles not fused (1). 76. (Wetterer et al., (2000) 100) M. styloglossus inserts on lateral surface of tongue along much of its length (0); or inserts on posterolateral “comer” of tongue (1). 77. (Wetterer et al., (2000) 101) M. genioglossus inserts into ventral surface of tongue along more than half of its length (0); or inserts into posterir half to third of ventral surface of tongue ( l); or inserts into posterior quarter of ventral surface of tongue (2). 78. (Wetterer et al., (2000) 102) M. stylohyoideus absent (0); or present (1); or sometimes present, polymorphic within species (2). 79. (Wetterer et al., (2000) 103) Anterolateral slip of m. sphincter colli profundus present (0); or absent (1). 27 80. (Wetterer et al., (2000) 104) Lateral slip of m. sphincter colli profundus passes laterally (0); or passes anterolaterally to insert on skin of cervical region (1). 81. (Wetterer et al., (2000) 106) M. cricopharyngeus consists of a single large slip (O), or two slips (1), or three slips (2), or more than three slips (3). 82. (Wetterer et al., (2000) 107) Medial circumvallate papillae present (0); or absent (1 ). 83. (Wetterer et al., (2000) 109) Lateral circumvallate papillae present (0); or absent (1). 84. (Wetterer et al., (2000) 112) Lingual sulci absent (0); or lateral lingual sulci present (1); or ventral lingual sulci present (2). 85. (Wetterer et al., (2000) 113) Brush of hairlike papillae around the distal margin of tongue absent (0); or present (1). 86. (Wetterer et al., (2000) 114) Hairlike papillae confined to lateral margin of distal third of tongue, with a single line of papillae that extends roughly to lateral circumvallate papillae (0); or hairlike papillae distributed around lateral margin and dorsum of distal third of tongue, not arranged in a single line (1). 87. (Wetterer et al., (2000) 115) Hairlike papillae fleshy and conical (0); or fleshy and conical with filamentous tips (1); or cylindrical with elipse-shaped distal end (2). 88. (Wetterer et al., (2000) 117) Small patch of anteriorly directed medial-posterior mechanical papillae always absent, all papillae oriented toward pharyngeal region (0); or media] patch present in some individuals, polymorphic within species (1); or medial patch always present (2). 89. (Wetterer et al., (2000) 119) Basketlike medial-posterior mechanical papillae absent (0); or present (1). 90. (Wetterer et al., (2000) 120) Cluster of horny papillae located near tip of tongue (0); or located significantly proximal to tongue tip (1). 91. (Wetterer et al., (2000) 124) Single large horny papilla present in center of 28 elliptical cluster (0); or two large horny papillae present in center of elliptical cluster (1). 92. (Wetterer et al., (2000) 125) Three small papillae present anterior to main papilla(e) (0); or one papilla present (1); or no papillae present (2). 93. (Wetterer et al., (2000) 126) Two or more small horny papillae present posterior to main papilla(e) (0); or absent (1). 94. (Wetterer et al., (2000) 127) Main horny papilla(e) flanked by a pair of smaller horny papillae, one on each side (0); or no papillae present lateral to main papilla(e) (1). 95. (Wetterer et al., (2000) 128) Paired lingual arteries present, lingual veins not enlarged (0); or single, midline artery present, lingual veins enlarged (1). 96. (Wetterer et al., (2000)l35) Accessory olfactory bulb absent (0); or present (1). 97. (Wetterer et al., (2000) 136) Cerebellar vermis does not cover medial longitudi- nal fissure or inferior colliculi (0); or cerebellar vermis completely covers longitudinal fissure between inferior colliculi, inferior colliculi exposed dorsally only along lateral edges of cerebellar vermis (1); or inferior colliculi completely covered by cerebellar vermis and cerebral hemispheres, colliculi not visible in dorsal view (2). 98. (Wetterer et al., (2000) 145) Restriction site 49 present (0); or absent (1). 99. (Wetterer et al., (2000) 146) Restriction site 50 present (0); or absent (1). 100. (Wetterer et al., (2000) 147) Restriction site 52 present (0); or absent (1). 101. (Wetterer et al., (2000) 148) Restriction site 53 present (0); or absent (1). 102. (Wetterer et al., (2000) 149) Restriction site 54 present (0); or absent (1). 103. (Wetterer et al., (2000) 1) Pelage differentiated into over hair and under hair (0); or pelage uniform, over hairs apparently absent (1). 104. (Wetterer et al., (2000) 4) Majority of scale margins on each hair entire (0); or irregular (1); or toothed (2); or entire and irregular (3); or entire and hastate (4). 105. (Wetterer et al., (2000) 5) Dorsal fur unicolored (O); or distinctly bicolored, hairs with pale bases and dark tips (1); or tricolored, hairs with distinct dark bases, a pale median band, and dark tips (2). 29 106. (Wetterer et al., (2000) 10) Uropatagium without fringe of hair along trailing edge (0); or with distinct fringe of hair along trailing edge (1). 107. (Wetterer et al., (2000) 12) Genal vibrissae absent (0); or one vibrissa present in each cluster (1); or two genal vibrissae present in each cluster (2). 108. (Wetterer et al., (2000) 13) Interramal vibrissae always absent (0); or none or one interramal vibrissa present, polymorphic within species (1); or one interramal vibrissa always present (2); or one or two interramal vibrissae present, polymorphic within species (3); or two interramal vibrissae always present (4); or none or two interramal vibrissae present, polymorphic within species (5); or three interramal vibrissae always present (6). 109. (Wetterer et al., (2000) 14) Vibrissae lateral to nose/ noseleaf arranged in two columns; medial column with three or more vibrissae, lateral column with two vibrissae (0); or single column with three or more vibrissae present, lateral column absent (1). 110. (Wetterer et al., (2000) 17) Padlike or flaplike vibrissa] papillae not in contact across dorsum of snout (0); or pads touch, or are confluent across dorsum of snout (l). 111. (Wetterer et al., (2000)]9) Noseleaf spear long, greater than twice the height of the horseshoe (0); or spear truncated, equal to or less than the height of the horseshoe (l). 112. (Wetterer etal., (2000) 20) Spear of noseleaf with pointed or rounded distal tip (0); or with u-shaped notch in distal tip (1). 113. (Wetterer et al., (2000) 21) Central rib absent (0); or rib restricted to proximal part of spear (1); or rib extends to distal tip of spear (2). 114. (Wetterer et al., (2000) 22) Intemarial region smooth, no midsagittal ridge or paillae (O); or narrow fleshy ridge or line of papillae always present along midsagittal line (1); or intemarial ridge or papillae variably present, polymorphic within species (2). 115. (Wetterer et al., (2000) 24) Lateral edges of horseshoe thin and free (0); or superior portion of swollen edge of horseshoe forms free, flap-like edge (1); or swollen 30 lateral edges of horseshoe ridgelike, fused to face along entire length with no free edge (2). 116. (Wetterer etal., (2000) 25) Inferior border of horseshoe is thin, free flap of skin (0); or inferior horseshoe is thickened ridge with no free edge (1); or inferior horseshoe grades smoothly into upper lip, no distinct boundary between lip and horseshoe (2). 117. (Wetterer et al., (2000) 30) Chin with pair of dermal pads, one present on each side of midline (0); or chin with multiple, well-developed dermal papillae (l); or chin smooth or with a few poorly developed papillae (2); or chin partly or completely covered with skin flaps (3). 118. (Wetterer et al., (2000) 32) Chin without central cleft (O); or with slight to deep central cleft (l). 119. (Wetterer et al., (2000) 33) Central papilla absent from chin (0); or central papilla present on chin just ventral to midline of lower lip (1). The two parts of the data set were combined into a single matrix (119 characters*47 taxa). Character states were recorded using MacClade version 3.04b (Madison and Madison, 1995). The decision to combine the data was reached after testing the partitions of the data set with the partition homogeneity test in PAUP*4b4a (Swofford, 2000), which tests for character congruence among different partitions of the data. Ultimately, morphological data were combined and analyzed using a total evidence approach in order to provide the best test of phylogenetic relationships by using all of the available synapomorphies (Kluge, 1998). The data were subjected to a parsimony analysis using the heuristic search option in PAUP* with 20 random addition replicates and TBR branch swapping. All characters were unordered and equally weighted. PAUP* was used to calculate tree statistics, in- cluding CI, RI, RC and tree length, and the strict consensus of the most parsimonious 31 trees. Clade stability was assessed using bootstrap analysis (Felsenstein, 1985) and Bremer support analysis (Bremer, 1988). PAUP* was used to perform the bootstrap analysis, with 1000 replicates. Bremer decay indices were computed by performing a sequence of searches; each consecutive search was set with a tree length of one greater than the prior search. Strict consensus trees were computed for each tree length, and these were used to determine the number of additional steps required to break down a given clade. It has been suggested that the Glossophaginae are an artificial assemblage, and that the Glossophagini and Lonchophyllini have converged to a similar morphology because they share a feeding niche (Baker et al., 1967; Winkelman, 1971; Griffiths, 1982; Baker et al., 2000). In order to investigate this possibility, these data were partitioned. One partition consisted of 36 characters (Table 2) obviously associated with nectar feeding. A partition homogeneity test was performed to assess character congruence between these characters and the remainder of the data set. The morphological data were combined with 1363 base pairs from the RAG—2 gene downloaded from Gene Bank (AF316433-AF316479) (Baker et al., 2000). A permutation homogeneity test was performed on the two partitions, morphological and molecular, of this new data set. The complete data set was then searched for the most parsimonious tree. 32 Table 2: Characters most likely to be convergent due to feeding. #20. The presence of a median gap between the lower incisors. #21 The number of lower incisors. #23. Presence of a ‘u’-shaped depression to the crowns of the lower incisors. #41. The presence of a median gap between the upper inner incisors. #42. The presence of procumbent upper incisors. #44. The upper inner incisors being twice a high as the upper outer incisors. #66-81. Musculature of the hyoid region (Wetterer, et al., 2000). #82-95. Characters of the tongue (Wetterer, et al., 2000). 33 Results The complete morphological data matrix consisted of 119 characters coded for 35 ingroup and 6 outgroup taxa for a total of 4879 coded characters. Of these, 3.08% were scored as missing, 2.92% were scored with a ‘-’, and 0.47% were multi-state. Most of the missing data came from two species, Musonycteris harrisoni and Scleronycteris ega (Table 3). A PT F test for phylogenetic signal was statistically significant (P: 0.01). A heuristic search of the entire morphological data set identified 863 most parsimonious trees with a length of 343, a consistency index of 0.472, a retention index of 0.809, and a rescaled consistency index of 0.382. The strict consensus of these trees is shown (Figure 28). The monophyly of Glossophaginae, Brachyphyllinae, Phyllonycterinae, and the tribes Glossophagini and Lonchophyllini are well supported with Bremer decay indices greater than or equal to 6 and bootstrap values above 74. The tree also strongly supports the monophyly of each of the following genera: Anoura, Choerom'scus, Leptonycteris, Monophyllus, and Phyllonycteris. A partition homogeneity test, used to evaluate the character congruence between 36 characters of the tongue, hyoid, and incisors likely to be convergent (Table 2) and the remaining 83 characters was not significant (P=0.30), indicating that this partitioning of the characters is not any less prone to homoplasy than any random partition of 36 characters. While the phylogeny loses resolution, the Glossophaginae remain monophyletic without these 36 characters. 34 Table 3: Ingroup sampling completeness for morphological data. Species #sampled missing 1 state 2 state char "-" A. caudifer 47 2 110 2 5 A. cultrata 19 2 110 2 5 A. geoflroyi 44 2 109 3 5 A. latidens 7 2 105 6 6 B. cavernarum 20 0 116 0 3 B. nana 9 0 115 l 3 C. godmani 10 1 113 0 5 C. minor 19 l 114 0 4 C. periosus 1 l 114 0 4 C. mexicana 22 l 113 0 5 E. bombifrons 11 7 110 0 2 E. sezekorni l7 7 110 0 2 G. commissarisi 11 0 118 0 1 G. leachii 25 0 118 0 l G. longirostris 16 0 118 0 1 G. morenoi 9 O 118 0 l G. soricina 76 O 118 O 1 H. underwoodi l4 4 115 0 4 L. curasoae 25 O 117 0 2 L. nivalis 20 0 117 0 2 L. yerbabuenae 7 0 117 O 2 L. obscura 14 7 108 0 4 L. spurelli 33 2 l 16 0 l L. handleyi 4 1 117 0 1 L. hesperia 8 l 117 0 1 L. mordax 16 l 117 0 l L. robusta 19 l 117 0 1 L. thomasi 43 1 117 0 l M. plethodon 8 O 118 0 1 M. redmani 26 0 118 0 1 M. harrisoni 6 35 80 0 4 P. aphylla 4 1 116 0 2 P. poeyi 17 1 116 0 2 P. genovensium 3 8 109 0 2 S. ega 1 41 45 0 33 % complete 98.3 98.3 98.3 98.3 100 100 99.2 99.2 99.2 99.2 94.1 94.1 100 100 100 100 100 96.6 100 100 100 94.1 98.3 99.2 99.2 99.2 99.2 99.2 100 100 70.6 99.2 99.2 93.3 65.5 35 A. caudifer A. cultrata A. geoflroyi A. latidens Ch. godmani Glossophagini Ch. minor without lower Ch. periosus incisors C. mexicana Mu. harrisoni S. ega H. underwoodi Li. obscura G. commissarisi G. leachii G. soricina G. longirostris G. morenoi Le. curasoae Le. nivalis Le. yerbabuenae Mo. plethodon Mo. redmani Ln. spurelli Lo. handleyi Lo. hesperia Lo. mordax Lo. robusta Lo. thomasi Pl. genovensium Ca. perspicillata g 2:22,."an lErachyphyllinae E. bombifrons E. sezekorni P. aphylla P. poeyi D. rotundus Ma. californicus Ph. discolor Pt. parnelli Ar. jamacensis Glossophagini with lower incisors onchophyllini Phyllonycterinae Figure 28: A strict consensus of the 863 most parsimonious trees from an analysis of 119 skull and sofi tissue characters. Tree length=343, Consistency index=0.472, Retention index=0.809, Rescaled consistency index=0.382. Bremer support values are given above each non terminal clade. Bootstrap proportions from 1000 replicates are given below clades found in greater than 50% of the replicates. The outgroup is bolded. 36 Morphological character data matching the representatives of nineteen genera that were included in the study by Baker et al. (2000) were combined with RAG-2 sequence data from Baker et al., (2000). A partition homogeneity test detected significant character heterogeneity between the two partitions (P: 0.0100), but the decision to combine was made after observing that the same clades were identified by each phylogeny, and that the differences involved the topology of the relationship between the major clades (Glossophagini, Lonchophyllini, Brachyphyllinae, and Phyllonycterinae). A branch and bound search identified a single most parsimonious tree (Fig. 29) with a length of 539, a CI of 0.532, and RC of 0.353, and a R1 of 0.663. The topology of this tree is identical to the one identified by the search of the morphological data, and most clades are well supported. The clade uniting the Glossophaginae and the clade uniting the Phyllonycterinae + Brachyphylla to the Glossophaginae receive the weakest support (bootstrap values of 70 and 55, respectively). In order to compare the strength of support between the morphological and molecular data, the topologies of each consensus tree (i.e., those matching Fig. 1 and Fig. 28) were forced to match the most parsimonious topology identified by the other data set. The number of additional steps that this required was then calculated. To force the molecular data onto the topology identified by the morphological data, an additional 10 steps were needed, which increased the tree length by 0.77%. To force the morphological data onto the topology identified by the molecular data, an additional 18 steps were needed, which increased the tree length by 4.64%. While the topology identified by the morphological data is a slightly better fit to the total evidence because it identifies the 37 Anoura 5 —— Choeroniscus ... 8 90 12 Ch ' '5; 100 3 r— oeronycterzs ; m 50 83 Mason cteris ED '2 3 100 y g, g 85 . 3 «‘3' Hylonycterts g E Glossophaga 7 l 2 . Glossophagini with 70 97 lit—Leptonycterzs lower incisors 67 Monophyllus 1 2 6 Lzonycteris . . 55 Lonchophyllini 100 Lonchophylla Brachyphylla lBrachyphyllinae 2 77 20 -——Er0phylla Phyllonycterinae 100 . ~—- Phyllonycterzs Artibeus 1 58 Carollia 1 Desmodus 69 1 Macrotus Phyllostomus —10 changes Figure 29: The most parsimonious tree in a branch and bound search of 237 informative characters; 1 18 from the RAGZ nuclear gene, 119 morphological. Tree length =539, Consistency index=0.532, Retention index=0.663, and Rescaled consistency index=0.353. Bremer decay values are given above each clade, and bootstrap proportions from 1000 replicates are given below clades found in greater than 50% of the replicates. 38 Discussion The combined data presented here (Fig. 29) suggest a single origin within the Phyllostomidae for the three subfamilies that rely on nectar as a resource. These data support the monophyly of Brachyphyllinae, Glossophaginae, and Phyllonycterinae. Additionally, there is support for the division of the Glossophaginae into two tribes, the Glossophagini and the Lonchophyllini (Wetterer et al., 2000). Support is strong for the separation of the Glossophagini into two clades, composed of glossophagines with lower incisors and glossophagines without lower incisors (Fig. 28 and Fig. 29). The basal nodes of the phylogeny receive the weakest support, a result consistent with the history of controversy over the classification of this group. The combined data suggest that the Brachyphyllinae and the Phyllonycterinae form a clade, and that this clade is the sister taxon of the Glossophaginae (Fig. 29). While the support for the clade uniting these subfamilies is weak, the phylogeny suggests that predominant nectarivory has a single origin within the Phyllostomidae. The morphological data, when analyzed alone, do not support the monophyly of the clade composed of the three families of primary nectarivores (Fig. 28). The major differences in the topologies of published phylogenies for this group consistently involve the Brachyphyllinae and Phyllonycterinae, two subfamilies endemic to the Caribbean (Baker et al., 2000; Wetterer et al., 2000; Gimenez et al., 1996). This study joins a long list of others that have found strong support for nodes near the terminal taxa but weak support in basal relationships of these groups. The available data are of limited use in uncovering the relationships between the three subfamilies of primary nectarivores. Uncertainty regarding these relationships complicates description of mor- 39 phological change during the evolution of nectarivory in the Phyllostomidae, but clear patterns to morphological changes involved in nectar feeding are evident within the Glossophaginae. This study joins recent studies in dividing the Glossophaginae into three major clades (Wetterer et al., 2000; Baker et al., 2000). One is the tribe Lonchophyllini, com- posed of the genus Lonchophylla and two monotypic genera associated with it, Lionycteris and Platalina. The second clade contains Glossophaga, Leptonycteris, and Monophyllus; all are glossophagines with lower incisors. The third is composed of glossophagines that lack the lower incisors: Anoura, Choeroniscus, Choeronycteris, Hylonycteris Lichonycteris, Musonycteris, and Scleronycteris. To facilitate discussion of character evolution I will refer to these as the Glossophaga-clade, and the Anoura-clade. When characters involved in nectar feeding are mapped onto the phylogeny (Fig. 30) they show a trend to increase the space available at the front of the mouth from the Lonchophyllini to the Anoura-clade. The most notable cause of this increase is the reduction of the lower incisors, which progress from the large lower incisors of most phyllostomid bats to the missing incisors of the Anoura-clade. Lonchophyllines have incisors that are relatively robust, with level crowns that fill the space available between the canines. The Glossophaga-clade has incisors that are reduced in size in comparison to the Lonchophyllini. The four incisors are approximately equal in size, but the inner incisors are at a lower elevation due to the shape of front of the mandible, resulting in a u-shaped depression in the crowns. The Caribbean genera Emphylla and Phyllonycteris apparently represent an independent evolution of the ‘u’-shaped depression in the lower incisors. The lower incisors of 40 ‘ _ w ' \ l Iii‘m'lij‘p/rr/lu upper incisors procumbent trifid lower incisors Outgroup (i/m sup/mgr: v 3* _ , . ;. a u-shaped , depressron [,r'pmn) mm , to lower incisors space between upper and lower incisors loss of trifid lower incisors and procum- bent upper incisors space between upper incisors loss of lower incisors Figure 30: The frontal gap. 41 Leptonycteris and Monophyllus have migrated laterally, forming a medial gap between the lower incisors. In the Anoura-clade the lower incisors are lost completely, and the front of the mandible is reduced as well, to its delicate condition in some taxa. A similar pattern of reduction is seen in the upper incisors. Brachyphylla has large incisors with pointed crowns that are similar in appearance to those of Carollia. The Lonchophyllini have incisors that are not reduced, but procumbent. This also increases the space available at the front of the mouth for the tongue to pass through, but in a different manner than the Glossophagini. The upper incisors of the Glossophagini re- duced to small pegs. Leptonycteris curasoae, Monophyllus redmani, and the Anoura- clade also have a median gap between their upper incisors, which further increases the space at the front of the mouth. While the reduction in the upper incisors does not ulti— mately result in the loss of teeth, it appears that the upper incisors in the Glossophagini are moving down the same evolutionary path as that traveled by the lower incisors. Indeed, some individuals were apparently born with only a single pair of upper incisors (Fig. 31). Overall, the pattern of incisor reduction increases the open space at the front of the mouth, which facilitates the movement of the tongue during feeding (Freeman, 1995). The importance of space at the front of the mouth is supported by the pattern of wear on the canines. Members of the Glossophaginae exhibit Figure 31: Single upper incisors in Choeroniscus minor. thegosis on the anterior face of their upper canines. According to Freeman (1995), “there is a tendency for the entire face of the canine to be worn in those bats without a frontal gap and a 42 smaller, usually cingular, patch of wear in those bats with large gaps. Tooth-on-tooth wear could result from the bracing of the lower teeth on upper to support the jaw during the rapid movement of the tongue at feeding”. The implication is that robust incisors can interfere with the movement of the tongue through the front of the mouth during feeding. Members of the Anoura-clade have less wear on the face of their upper canines than do; other glossophagines, because the need to brace their mouth open with their canines is not nearly as great. The pattern of morphological change in the dental characters at the front of the rostrum shows increasing specialization within the Glossophaginae, but other types of cranial characters do not vary in a similar pattern on the phylogeny. Losses of cheekteeth are common; a lower premolar is lost at the level of the last common ancestor of Phyllonycterinae and Brachyphyllinae, an upper premolar is lost at the last common ancestor of Anoura spp., an upper and lower molar is lost at the last common ancestor of Leptonycteris spp., and an upper and lower molar is also lost in Lichonycteris obscura. Many dental characters in the nectar-feeding phyllostomid bats are reductions in size or complexity from the ancestral state. The width of the lower premolars is apparently reduced at the last common ancestor of the genera Choeroniscus, Choeronycteris, Musonycteris, and Scleronycteris. Molars are apparently reduced in complexity at several nodes of the phylogeny, and this reduction can take the form of a lost metaconid, entoconid, or paraconid, lost cingular shelves, and reductions of the ‘w’- shaped ectoloph. These reductions consistently occur near the terminal taxa (Fig. 28) and are synapomorphies for many genera. However, there is no pattern to these beyond a general trend towards reduction, and these reductions do not act as synapomorphies for larger clades. 43 Several cranial characters also exhibit homoplasy. One is the presence of three major foramina in the premaxillary region in most members of the Glossophaginae. These are arranged in a triangle; one small foramen is proximal to the incisors and two larger paired foramina are posterior to the first. In what are apparently independent reversals to the ancestral state, three taxa lack the small foramen nearest the incisors; these include Lichonycteris obscura, Scleronycteris ego and Lionycteris spurelli. In the genera Anoura and Choeroniscus, the small foramen has migrated forward and is located between the two upper incisors, contributing to the spacing between them. This migration of the foremost foramen has apparently occurred independently in Choeroniscus and Anoura. Some museum specimens have an incompletely formed premaxilla, resulting in a ‘v’- shaped indentation in the anterior margin of the premaxilla between the incisors. In the species examined here the zygomatic is reduced, and in many taxa is lost completely (Fig. 32). This loss has apparently occurred three times: in the last common ancestor of Phyllonycteris, in Lonchophylla, and in the Anoura-clade. Reduction of cranial and dental characters is common in nectar-feeding phyllostomid bats, but, with the exception of the incisors, there is no apparent pattern to these reductions. Body mass is a significant constraint in flying vertebrates, and hovering flight may increase the selective pressure for reduced mass in nectarivores. Glossophagine bats are capable of hovering for several seconds at a time (Winter, 1998; pers. obs.), and hovering is the most energetically expensive type of flight (Bicudo and Zerbinatti, 1995). Both the required oxygen uptake and the power that the hovering bat must generate increase linearly with mass, and there may be additional constraints on the center of gravity in the hovering bat (Voight and Winter, 1999). The teeth are the structure 44 in mammals with the most density, and the reduction in dentition may be related to selection for increased efficiency while ‘ [hm/n-p/n'I/a mtmmrmn hovering. This would explain the general & 1..., _ lack of pattern in the reductions; in teeth that ) . . . , .' . . are of limited use in processing food it I I'll/UH“ " H" UNIV/N probably does not matter how the reduction occurs, only that it does. This is contrasted . . . LIUII('\'/(‘I'l.\' .\'/)lll'(‘//l with the incisors, where the corollas of the m a,“ flowers and the specialized tongue morphol- ogy make the reduction of the incisors ,‘IIUHHIIIII‘HILY [1/(‘l/Im/UII doubly adaptive. Reduction in the incisors is related to the use of the tongue, but also consistent with l-(‘I’Wll'i"("71" ”I'm/I7" the theory that selection for reduced mass is particularly important in hovering glossophagines. In order to evaluate the importance of these selective pressures, the diversity of diet within the Glossophaginae should be considered. The loss of the incisors does not force specialization on nectar onto glossophagine bats; Anoura IS a genus com— (‘hm'mnm-m [NW-mm. posed of dietary generalists, Choeroniscus Figure 32; Reduction of zygomatic. 45 spp. and Hylonycteris underwoodi are known to include fruits as a part of their diet (Nowak, 1994). Nor does the presence of lower incisors prevent specialization, as a comparison between Platalina genovensium and Choeronycteris mexicana illustrates. Both species live in arid regions, are cactophilic, and are among the heaviest nectarivorous bats (Simmons and Wetterer, in press; Sahley and Baraybar, 1995). The premolars, canines, and skulls of these species are similar in size and form, but the incisors of Platalina are among the most robust of the Glossophaginae while the incisors of Choeronycteris are among the most reduced. The incisors of Platalina suggest both that it is possible for the tongue to reach nectar and the bat to hover without reduced incisors. The reduction in the incisors and elongation of the rostrum in nectar feeding bats is influenced by coevolution between the corollas of their host plants and the length of the rostrum. If the frontal gap does facilitate the movement of the tongue, as Freeman sug- gests, there are immediate and delayed selective advantages. The immediate advantage is increased feeding efficiency and results in higher survival. The delayed advantage may result from the opening of new feeding niches. Nectarivorous bats co-occur with hum- mingbirds throughout their range and feed on some of the same plants (Sazima et al., 1994). Several plant species have evolved chiropterophily from hummingbird-pollinated ancestors (Sazima et al., 1994). Flowers pollinated by hummingbirds have long narrow corollas (Procter et al., 1996), and the nectar in flowers with morphology adapted to hummingbird pollinators may only be reachable if the tongue can pass out of the mouth without opening the it. Field observations that correlate the morphology of bat pollinators to the corollas of their host plants are needed to further investigate these ideas. 46 Specialization on nectar as a resource was made possible by dental reduction in the front of the mouth and concurrent changes that increased the effectiveness of the tongue in feeding. Species with a large frontal gap may have access to food sources (flowers adapted to hummingbird pollinators) that are not available to taxa. The Glossophaginae has benefited from incisor reduction because the advantage gained by opening new feeding niches has outweighed the increased difficulty in consuming other food sources. 47 APPENDIX 1: SPECIMENS EXAMINED Anoura caudifer NMNH419463, NMNH517413, NMNH517409, NMNH444712, NMNH517412, NMNH517415, NMNH517418, FMNH138885, FMNH138886, FMNH138889, FMNH138891, FMNH65641, FMNH66372, FMNH93541, FMNH141596, FMNH141597, FMNH124684, FMNH113502, FMNH138866, FMNH138865, FMNH113503, FMNH113502, FMNH113504, FMNH113504, FMNH113503, FMNH113502, FMNH93543, FMNH66372, FMNH65641, FMNH66367, FMNH66368, FMNH66369, FMNH66370, FMNH68373, FMNH66374, FMNH68374, FMNH75144, FMNH75145, FMNH75146, FMNH75147, FMNH75148, FMNH93539, FMNH93540, FMNH93541 , FMNH93542, AMNH 176347, AMNH212261 Anoura cultrata NMNH337987, NMNH309401, NMNH309398, NMNH562784, NMNH562781, NMNH562774, N MNH562776, FMNH58797, FMNH58799, FMNH58790, FMNH58795, FMNH58798, FMNH48789, FMNH58791, FMNH58792, FMNH58793. FMNH58794, FMNH58796, AMNH233257 Anoura geoffroyi MSU13987, MSU16118, MSU16119, MSU16120, MSU8801, MSU8161, MSU17113, MSU22076, MSU22077, MSU22078, MSU3241. MSU905, MSU23485, MSU23486, MSU8798, MSU8800, MSU20551, MSU31943, MSU31946, FMNH128640, FWH128642, FMNH128643, FMNH128645, FMNH73362, FMNH41831, FMNH41832, FMNH41833, FMNH41834, FMNH41835, FMNH41837, FMNH41838, FMNH41654, FMNH64662, FMNH128643, FMNH 128645, FMNH137241, FMNH137242, AMNH60538. AMNH203678 Anoura latidens NMNH370116, NMNH370115, NMNH370114, NMNH370112, NMNH370111, NMNH3701 18.NMNH370122 Artibeus jamaicensis FMNH108323, FMNH108327, AMNH39101, AMNH72247, AMNH248510 Brachyphylla cavemarum NMNH544832, NMNH544830, NMNH 104062, NMNH 104060, NMNH104063, NMNH104064, NMNH58067, MSU2848, MSU2846, FMNH104596. AMNH39287, AMNH7227 8, AMNH72294, AMNH72295, AMNH213706, AMNH213731, AMNH213735, AMNH246997, AMNH246998, AMNH246999 48 Brachyphylla nana NMNH538175, NMNH538176, NMNH538177, NMNH538178, NMNH538179, NMNH539740, NMNH539741, AMNH175972, AMNH175973 Carollia perspicillata FMNH120796, AMNH202299, AMNH212944, AMNH217534, AMNH5217535, AMNH266130, AMNH266149, NMNH536905, NMNH537910 Choeroniscus godmani NMNH574513, NMNH582302, NMNH582303, NMNH524402, NMNH524403, NMNH337551, NMNH337550, AMNH172778, AMNH172779, AMNH186162 Choeroniscus minor NMNH361573, NMNH361574, NMNH361575, NMNH460100, NMNH460101, NMNH460102. NMNH460103, FMNH74255, FMNH74258, FMNH74262, AMNH230285, AMNH230286, ANH179956, AMNH185314, AMNH266120, AMNH266377, AMNH140471, AMNH385925, AMNH460101 Choeroniscus periosus AMNH2 1703 8 Choeronycteris mexicana UMMZ77767, MSU894, MSU895, MSU897, MSU898, MSU899, MSU39889, MSU15356, MSU25267, MSU25268, MSU8795, MSU902, MSU904, MSU15355, MSU23488, MSU23489, MSU23490, FMNH43772, AMNH173665, AMNH173871, AMNH212359, AMNH212364 ' Desmodus rotundus FMNH58273, AMNH172293, AMNH174303, AMNH189215, AMNH190149, AMNH208894, AMNH208897, AMNH267211 Erophylla bombifrons NMNH395164, NMNH538347, NMNH538348, NMNH238321, NMNH538320, NMNH252618, NMNH253634, AMNH39340, AMNH3939, AMNH39345, AMNH39346, Erophylla sezekorni NMNH102050, NMNH102051, NMNH102052, NMNH102053, NMNH102055, NMNH102053, AMNH41062, AMNH41059, AMNH41070, AMNH41063, AMNH41703, AMNH4824, AMNH41056, AMNH41057, AMNH41064, AMNH167115, AMNH194201 Glossophaga commissarisi MSU4766, MSU5697, MSU8154, MSU22547, MSU4768, MSU15627, FMNH10878 1, FMNH108786, FMNH108787, AMNH189605, AMNH235715 49 Glossophaga leachii MSU13980, MSU11308, MSU11312, MSU4764, MSU3276, MSU8152, MSU38, MSU16110, MSU16112, MSU12611, MSU16108, MSU10263, MSU37, FMNH61627, FMNH61628, FMNH61629, FMNH61630, FMNH61631, FMNH61632, FMNH61633, FMNH61634, FMNH61635, AMNH97545, AMNH135277, AMNH189626 Glossophaga longirostris FMNH21942, FMNH21943 , FMNH3727, FMNH122066, FMNH122065, FMNH69442, FMNH51178, FMNH21943, FMNH51177, FMNH14890, FMNH21942, FMNH14893. FMNH21926, AMNH182724, AMNH182725, AMNH182904 Glossophaga mexicana NMNH6992, NMNH332721, NMNH332722, NMNH559499, NMNH559500, NMNH559501, MSU13984, MSU13976, MSU12610 Glossophaga soricina MSU32866, MSU11841, MSU32865, MSU32864, MSU32863, MSU32862, MSU32861, MSU28094, MSU28104, MSU28096, MSU28093, MSU2809, MSU28091, MSU30765, MSU28972, MSU28974, MSU28975, MSU28976, MSU28977, MSU28978, MSU28979, MSU28969, MSU28970, MSU28973, MSU28968, MSU2897 l, UMM2124356, UMM2124357, UMM2125874, UMM2125875, FMNH126861, FMNH126868, FMNH74114, FMNH58578, FMNH126856, FMNH126849, FMNH128678, FMNH124686, FMNH128660, FMNH150624, FMNH58578, FMNH74110, FMNH74111, FMNH74112, FMNH74113, FMNH74114, FMNH106769, FMNH58172, FMNH58173, FMNH58174, FMNH106770, FMNH108771, FMNH108773, FMNH108774, FMNH108775, FMNH114880, FMNH114879, FMNH114881, FMNH114882, FMNH114883, FMNH114884., FMNH114886, FMNH114887, FMNH114888, FMNH81085, FMNH81086, FMNH81087, FMNH81088, FMNH81089, FMNH81090, FMNH81092, FMNH81091, FMNH81093, AMNH91929, AMNH214415, AMNH214417 Hylonycteris underwoodi UMMZl 13582, NMNH562787, NMNH562788, NMNH562789, NMNH562790, NMNH562791, NMNH562792, NMNH562793, NMNH457939, NMNH541067, AMNH178904, AMNH189687, AMNH189688, AMNH238199 Leptonycteris curasoae MSU41, MSU40, MSU16487, MSU13989, MSU8797, MSU26403, MSU12615, NMNH444777, NMNH444778, NMNH444779, NMNH444780, NMNH455151, NMNH455153, NMNH455154, FMNH4377 1 , AMN H7402, AMNH7403, AMN H27 32 1 , AMNH149385, AMNH149390, AMNH169966, AMNH173667, AMNH173669, AMNH180347, AMNH180349, AMNH189701 Leptonycteris nivalis 50 NMNH511306, NMNH511307, NMNH511308, NMNH556307, NMNH556309, NMNH556309, NMNH556312, NMNH556313, UMM2108501, UMM2108506, UMMZIO8509, UMMZ25264, UMMZI6488, FMNH46887, FMNH46888, FMNH121253, FMNH121252, FMNH121254, AMNH172039, AMNH249086 Leptonycteris sanborni UMMZ9191], UMM2183032, UMM2183044, UMMZI83052, UMM2183052, NMNH559576, NMNH314690 Lichonycteris obscura NMNH362595, NMNH396476, NMNH537589, NMNH575499, NMNH309403. NMNH315310, NMNH331258, FMNH34951, FMNH69867, AMNH131769, AMNH24462 l , AMNH95485, AMNH13 1769, AMNH267960 Lionycteris spurelli NMNH407819, NMNH407820, NMNH407821, NMNH407822, NMNH407823, NMNH407824, NMNH407825, FMNH138810, UMMZI60715, UMMZI60714, UMMZI60713, UMMZI60712, AMNH230209, AMNH26004, AMNH230207, FMNH138910, AMNH78431, AMNH78433, AMNH78434, AMNH97221, AMNH97264, AMNH97267, AMNH97269, AMNH202295, AMNH230207, AMNH230209, AMNH236010, AMNH236014, AMNH236016, AMNH236019, AMNH236022, AMNH236024, AMNH236027 Lonchophylla handleyi NMNH507172, N MNH364347, AMNH230215, AMNH230214 Lonchophylla hesperia FMNH81 103, FMNH128721, FMNH128720, NMNH283177, FMNH 128720, FMNH128721, FMNH128721, FMNH128720 Lonchophylla mordax UMMZl68884, NMNH528494, NMNH528495, NMNH528496, NMNH528497, NMNH528498, NMNH528500, FMNH136855, FMNH136858, FMNH21078, FMNH21077, FMNH136857, FMNH136858, FMNH136855, FMNH136856, FMNH136859 Lonchophylla robusta UMMZl 12035, UMM2112036, NMNH3] 199, NMNH312000, NMNH313747, NMNH3 13749, NMNH315306, NMNH315304, NMNH315305, FMNH34068, FMNH51732, FMNH34068, FMNH51332, AMNH143761, AMNH143762, AMNH143763, AMNH185380, AMNH233761, AMNH233179 51 Lonchophylla thomasi UMMZI60708, UMMZI60710, MSU32858, NMNH385753, NMNH385752, N MNH407796, NMNH407797, NMNH407798, NMNH407801, NMNH407802, FMNH13891], FMNH87070, FMNH123847, FMNH13891 1, FMNH125465, FMNH125462, FMNH123847, FMNH87070, AMNH95493, AMNH95772, AMNH97271, AMNH97272, AMNH209358, AMNH210688, AMNH262429, AMNH262434, AMNH266100, AMNH266104, AMNH266107, AMNH266108, AMNH266117, AMNH Macrotus californicus NMNH139584, NMNH139586, NMNH 146039, NMNH 146040, NMNH 146041, NMNH146042, NMNH145937, FMNH52798 Monophyllus redmani UMM2123278, FMNH14895, NMNH520515, NMNH520516, NMNH520514, NMNH238346, NMNH219152, NMNH253646, NMNH300585, NMNH534893, NMNH534899, NMNH534900, AMNH19106, AMNH23782, AMNH23783, AMNH39431, AMNH39436, AMNH39439, AMNH39440, AMNH39444, AMNH39447, AMNH39519, AMNH39522, AMNH39525, AMNH219658, AMNH219660 Monophyllus plethodon NMNH544812, NMNH548 1 1, NMNH544810, NMNH544809, NMNH361896, NMNH361897, NMNH362097, AMNH72367 Mormoops megalophylla NMNH508478, NMNH508480, NMNH508481, NMNH508482, NMNH511284, NMNH51 1285, NMNH523067 Musonycteris harrisoni UMM2110524, FMNH142624, FMNH142623, NMNH314639, NMNH324971, AMNH235179 Platalina genovensium FMNH24336, NMNH268765, AMNH257108 Phyllonycteris aphylla NMNH545186, NMNH545188, NMNH545187, AMNH214130 Phyllonycteris poeyi NMNH103537, NMNH103541, NMNH103546, NMNH103547, NMNH103548, NMNH103549, NMNH103550, NMNH538349, AMNH176028, AMNH103545, AMNH 176027, AMNH 176026, FMNH 14892, AMNH 10749, AMNH23758. AMNH176019, AMNH236697 52 Phyllostomus discolor FMNH 1 36884 Pteronotus parnellii NMNH523038, NMNH523039, NMNH523040, NMNH523041, NMNH523042, NMNH523044, MNH523045, AMNH30660, AMNH260001, AMNH260002. AMNH30651, AMNH30652, AMNH30654, AMNH30655, FMNH106765, FMNH58135 Scleronycteris ega N MNH407889 53 caudifer cultrata geoftnoyi latiden- jalaicenlil cavernaru- nana ,perqpicillata god-uni lino: patio-u- lexicana rotundu- banbifrone sezekorni oanniaaarili leachii longirOItrie .loren01 noricina underuoodi curasoae alvalil yerbabuenae obscura spurelli handlqyi heeperla .lordax robust. tho-all californiaul p1 ethodon rod-uni harrisoni aphylla poeyi discolor genovenelul parnelli ego AJHHHWDEKIBIMKLABHAITHXL Cranial characters (1-19) 1 21011 21211 21211 21011 11200 12200 12200 11000 11010 11010 11010 01010 21200 12000 11000 11010 11010 11010 11010 11010 11010 11211 21211 11211 11001 11000 11010 11010 11010 11010 11010 01100 11011 11011 11010 22000 22000 00000 11010 00000 -1000 6 01001 01001 01001 01001 00000 00001 00001 00001 01100 01100 01100 10000 00001 00000 00000 00000 00001 00001 00001 00001 00101 00001 00001 00001 00101 00000 00000 00000 00000 00000 00000 00001 00001 00001 10000 00010 00010 00000 00000 00000 10000 1 1 01000 01000 01000 01000 00000 00000 00000 00000 00100 00100 00100 00101 00000 00000 00000 00010 10010 00010 00010 10010 00010 00010 00010 00010 00000 00000 00000 00000 00000 00000 00000 00000 00000 00000 00101 00000 00000 00000 00000 00000 00000 1 6 1(01)oo 1(01)oo 1(01)oo 1000 0110 0110 0110 1010 1000 1000 1000 1000 1110 0101 0101 1100 1100 1100 1100 1100 1000 0100 0100 0100 0000 1001 1001 1001 1001 1001 1001' 1110 1100 1100 1000 0001 0001 1110 1001 0110 1100 caudifer cultrata gooffroyi latiden- jalaiconaio oavornaru- nana ,poropiolllata god-uni .linor ,porioouo .loxicona rotundu- bonbifrono sezekorni oomniooarioi Jonquil longirootrio .loronoi oorioina underwoodi curasoae nivalio yorbobuonao obscura spurelli handloyi hooperia .Iordax robuota tho-all oolifornioul p1 ethodon rod-an1 harrlooni aphylla ,pooyi discolor gonovonoiul ,pornelli ego .APPENDEXIBIMKDARLNTREK Dental characters (20-50) 2 2 3 0 6 1 -0—100 30000 30000 -0--10 13000 03000 -0--10 (01)3000 03100 -0--10 03000 03100 020000 12000 03000 020100 12100 03000 020100 12100 03000 020000 12000 03000 -0--10 03011 03000 -0--10 03011 03000 -0--10 03011 03000 -0--11 13001 03000 121000 01000 02--0 020100 12000 03010 020100 12000 03010 022111 13000 03000 022111 13000 03000 022111 13000 03000 022111 13000 03000 022111 13000 03000 -0--10 13000 03000 020011 13000 12001 120111 13000 12001 120111 13000 12001 -0--00 03000 02000 021011 03100 03100 021011 13000 03100 021011 13000 03100 021011 13000 03100 021011 13000 03100 021011 13000 03100 020000 13000 03000 020110 13000 03001 020110 13000 03001 -0--11 13001 03000 020100 12000 03010 020100 12000 03010 020000 12000 03000 020011 13000 03000 02100- 13000 03000 -0--00 13001 03001 55 3 6 00001 00000 00000 00000 00000 00011 00011 10010 10000 10000 10000 10100 00000 00000 00000 00000 00000 00000 00000 00000 00000 00000 00000 00000 10000 01000 01000 00000 00000 01000 00000 10010 10000 10000 10100 00000 00000 10000 00000 00001 00100 4 1 01010 10101 10101 10100 00000 00010 00010 00110 10000 10000 10000 10000 00--0 00000 00000 00100 00100 00100 00100 00100 10000 00101 10101 00100 00000 01110 01110 01110 01110 01110 01110 00010 00101 10001 10000 00100 00100 00111 01110 00001 10000 4 6 30111 13011 03010 03011 12000 12100 12100 02000 02010 02010 02010 02010 00000 12000 12000 12010 12010 12010 02010 12010 02010 12011 12011 12010 02011 02011 02011 02011 02011 02011 02011 02001 12010 12010 02010 12000 12000 12001 02000 12001 02010 A. A. A. A. A. B. B. C. C. C. C. C. D. l. l. G. G. G. G. G. 8. L. L. L. L. L. L. L. L. L. L. I} I} H5 P. P. P. P. P. 8. caudifer cultrata gooffrqyl latidens ja-sloonsls oavornarul nana ,porsplolllats god-uni llnor ,porlosus lexicons rotundus bo-bltrons sezekorni col-lsssrdsl losohll longlrostris loronol soriclns undorwoodl curasoae nlvolls yorbsbuonso obscura spurelli handler! hosporls .lordsx robusts thomasi osllfornlous ,plethodon rod-nal harrisoni aphylla .poqri discolor gonovonslu- parnelll ago 5 1 131(01)0 13100 131(01)0 131(01)0 03002 03102 0(23)102 03100 13100 13100 13100 13100 1210- 13102 13102 13100 13100 13100 13100 13100 13100 12110 12110 12110 12100 13100 13110 13110 13110 13110 13110 13010 13210 13210 13100 13102 13102 03000 13100 03010 13100 5 6 00010 00(01)10 00(01)10 00110 -0000 10000 10000 00010 00000 00000 00000 00000 -0-00 01000 01000 00010 00010 00010 00010 00010 00010 00001 00001 00001 00000 00110 00110 00110 00110 00110 00110 00011 00010 00010 00000 01000 01000 00010 00100 00010 00001 6 1 01 01 01 01 00 10 10 00 00 00 00 00 00 00 00 00 00 00 00 00 00 00 00 00 00 10 10 10 10 10 10 00 00 00 00 00 00 01 10 10 00 .APPENDIXIBIMKDARLNIRDK Dental characters, cont. (51-62); Wing bones (63-65) 6 3 000 000 000 000 500 500 500 501 000 000 000 000 401 512 512 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 402 000 000 000 510 510 000 000 000 000 A. A. A. A. A. B. B. C. C. Co C. C. D. 8. G. C. C. G. H} L. L. L. L. L. L. L. L. L. L. I} I} I} I} P. P. P. P. P. 8. APPENDIX 11: DATA MATRIX Hyoid musculature (66-81); Tongue (82-95) caudifer cultrata gooftroyl latidens ja-sloonsls osvornsrul nana ,porsplolllsts god-sol lunar ,porlosus .loxloons rotundus bolblfrons sezekorni con-lssarlsl losohll longlrostrls .loronol sorlolna undoruoodl curasoae nlvslls yorbsbuonse obscura spurelli handloyl hosporla .lordsx robusts thomasi oollfornlous plethodon rod-sol harrisoni aphylla ,pooyl discolor gonoronslu- ,psrnolll ogs uuwwwwwwwwwupa ”OHNHHMNMNHHHHHwaNUMUMWUwHt-J 8 2 1001 1001 1001 1001 0000 0100 0100 0000 1001 1001 1001 1001 0000 0001 0001 0001 0001 0001 0001 0001 1001 0001 0001 0001 1001 0011 0011 0011 0011 0011 0011 0000 0001 0001 ???? 0001 0001 0000 0011 0000 ???? 8 6 11001 11001 11001 11001 ---00 --010 --010 —-010 11001 11001 11001 11001 --010 12000 12000 11001 11001 11001 11001 11001 11011 11001 11001 11001 11011 00210 00110 00110 00110 00110 00110 --010 11001 11001 ????? 12000 12000 --010 00200 ---10 ????? Brain (96-97); rDNA Restriction site (98-102); Pelage (103-119). caudifer cultrata gooffroyl latidens jalslconsls csvsrnsru- nana ,porsplclllsts god-sol minor ,porlosus .loxlcsns rotundus bo-blfrons sezekorni colnlsssrlsl loschli longlrostrls .loronol sorlclns undoruoodl curasoae nlvslls yorbsbuonss obscura spurelli handloyl hosporls .lordsx robusts thomasi csllfornlcus pl ethodon rod-nal harrisoni aphylla ,pooyl discolor gonovonslus parnelll ego APPENDIX II: DATA MATRIX 9 6 12 12 12 12 1- 02 02 12 02 02 02 ?2 02 ?1 ?1 12 12 12 12 12 ?2 12 12 12 ?2 1? 12 12 12 12 12 ?0 12 12 ?? ?1 ?1 1- ?? -1 ?? 9 8 000 000 000 000 000 000 000 000 101 101 101 101 000 ??? ??? 000 000 000 000 000 1?1 010 010 010 ??? 010 010 010 010 010 010 000 010 010 101 000 000 010 ??? ??? 1 0 1 00121 00121 00121 00121 00121 01001 01001 00102 00101 00101 00101 00101 00011 ??001 ??001 00101 00101 00101 00101 00101 ?0102 00121 00121 00121 ??102 10020 10101 10101 10101 10101 10101 01101 00100 00100 00??1 01011 01001 01011 ??101 --040 ????1 1 0 6 11400 11400 12400 1-400 02410 01401 01401 00410 0--00 00100 01200 01200 12400 01401 01401 00400 00400 00400 00400 00400 01400 11400 11400 11400 01400 01600 0-600 0-600 00600 02600 00600 02400 00400 00400 0020? 02401 02401 02010 00600 0120- 01?0? 1 1 1 00012 00012 00012 00012 00200 11000 11000 00110 00011 00011 00011 00011 11000 10000 10000 00012 00012 00012 00012 00012 00011 00012 00012 00012 00011 00112 00112 00112 00112 00112 00112 00010 00012 00012 00011 10000 10000 00200 00002 .__0. 00--- 1 1 6 201- 201- 201- 201- 0101 2100 2100 2101 201- 201- 201- 201- 2001 201- 201- 201- 201- 201- 201- 201- 201- 201- 201- 201- 201- 2000 2000 2000 2000 2000 2000 1000 201- 201- 201- 201- 201- 0100 2000 -30- 201- LITERATURE CITED Baker, R. 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