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Comparative Morphology and Evolution of the Female Reproductive Tract in Macroglossine Bats (Mammalia, Chiroptera) CRAIG S

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Comparative Morphology and Evolution of the Female Reproductive Tract in Macroglossine Bats (Mammalia, Chiroptera) CRAIG S JOURNAL OF MORPHOLOGY 199:207-221 (1989) Comparative Morphology and Evolution of the Female Reproductive Tract in Macroglossine Bats (Mammalia, Chiroptera) CRAIG S. HOOD Department of Biological Sciences and The Museum, Texas Tech University, Lubbock, Texas 79409 ABSTRACT Comparative morphological analysis of the female reproduc- tive tract in macroglossine bats was undertaken to test the hypothesis that nectarivory arose at least twice within Old World fruit bats. Given that features of the female reproductive tract are not directly involved in adap- tations for feeding, this data set should provide a test of the monophyly of macroglossine bats. A cladistic analysis of variation in the structure of the ovaries, oviducts, uterus, and external genitalia supports the hypothesis that Megaloglossus has developed a nectar-feeding habit independent of other macroglossine genera. Most of the variation in female reproductive organs among pteropodids is found in the development of derived external and in- ternal features of the uterus. Fusion of uterine cornua, expansion of the common uterine body, and elaboration of the cervical region are found in a group which includes species ofPteropus, Dobsonia, Nyctimene, and the ma- croglossines (excluding Megaloglossus). Results of this study are concordant with independent data sets, thus providing a phylogenetic framework to eval- uate critically structural and functional design in the evolution ofpteropodid feeding mechanisms. One of the most challenging problems in elongated and protrusible tongue. However, evolutionary biology is the understanding of most of these features (except those of the evolutionary change in the form and func- tongue and hyoid region) are not unique to tion of complex anatomical systems. In re- macroglossine bats, also occur in other pter- cent years, the fields of functional and evo- opodids that do not feed on nectar (Ander- lutionary morphology have been redirected sen, '12). by incorporating phylogenetic methods as Features of the female reproductive sys- tools to identify and interpret structural and tem have proven useful in assessing evolu- functional design (Lauder, '81, '82; Liem and tionary relationships within and among bat Wake, '85). This approach has been success- families (Wimsatt and Enders, '80; Luckett, fully applied to the study of feeding mech- '80; Hood and Smith, '82, '83). This report anisms in actinopterygian fish (e.g., Lauder, describes the system in pteropodid bats, as- '83; Schaefer and Lauder, '86) and pletho- sesses the monophyly of the subfamily Ma- dontid salamanders (e.g., Lombard and Wake, croglossinae, evaluates the fit of macroglos- '86; Wake and Larson, '87). sine bats within the larger context of the The chiropteran family Pteropodidae in- family Pteropodidae, and tests of concord- cludes 44 genera and about 173 species (Fig. ance among independent data sets. 1; Koopman, '84). Bats of the subfamily Ma- croglossinae have long been recognized as MATERIALS AND METHODS members of a monophyletic group on the ba- All specimens were collected in the wild sis of their adaptations to a nectarivorous (Table 1). The anatomical relationships of diet (Dobson, 1875; Andersen, '12; Koop- female reproductive organs and their asso- man, '84). Morphological adaptations asso- ciated with this highly specialized food habit Dr. Craig S. Hood is now at Dept. of Biological Sciences, Loyola include an elongated rostrum, modified University, New Orleans, LA 70118. Address reprint requests braincase, reduced dentition, and a highly there. © 1989 ALAN R. LISS, INC. 208 C.S. HOOD ' | ' Notoplerine Subfamily Subfamily Eonycterine Croup Pteropodinae Macroglossinae Group | Subfamily Macroglossinae Family Pteropodidae Rousen'ine Section Epomophorine Section Fig. 1. Phylogenetic relationships of the higher tax- onomic groups ofpteropodid bats implied by traditional classifications (after Andersen, '12). ciated supporting membranes were ascer- processed for SEM by fixation with 2% glu- tained by gross dissection at the time of cap- taraldehyde in 0.1 M phosphate buffer at pH ture and excision of tissues, or from dissection 7.2, dehydration, drying in a Parr 4770 crit- of specimens that were collected and pre- ical-point dryer, and gold-pallidium coating served intact. Whole reproductive tracts were at 300 A with a Technics Hummer V Sputter excised and fixed for gross anatomy, histol- Coater. They were observed with a Hitachi ogy, and scanning electron microscopy. S-570 scanning electron microscope at 20 kV. Voucher specimens have been deposited in Phylogenetic relationships were recon- the mammal collections of the American structed using cladistic methods, with out- Museum of Natural History; Carnegie Mu- group comparison and parsimony (Kluge and seum of Natural History; Museum of Com- Farris, '69; Watrous and Wheeler, '81; Far- parative Zoology, Harvard University; Nat- ris, '82; Maddison et al., '84; Smith and Hood, ural History Museum, Los Angeles County; '84). Outgroups examined included repre- Thailand Institute of Technology and Re- sentatives from all bat families except the search; and The Museum, Texas Tech Uni- Craseonycteridae, Furipteridae, and Myzo- versity. podidae. Data from the literature were used Tissues were fixed in 10% buffered for- to determine distribution of character states malin or Boulin's solution and then pro- in other mammalian orders. cessed through paraffin, serially sectioned at 6—10 (Jim, and stained with Mallory's Triple RESULTS Stain or Gomori's One Step Trichrome Gross morphology and external genitalia Method (Humason, '72; Thompson, '66; Hood The overall anatomical arrangement of the and Smith, '83). Selected reproductive tracts ovaries, oviducts, and uterus in pteropodid BAT REPRODUCTIVE TRACT MORPHOLOGY 209 TABLE 1. List of specimens examined in this study1 ids, and molossids (see also Wood Jones, '17; Family Pteropodidae Matthews, '41; Madkour, '76). Together with pteropodids, these bat families share a Subfamily Pteropodinae broadly flattened genital tubercle and cli- Rousettine-section Rousettus amplexicaudatus (5) toris, and an overall transverse disposition Pteropus admirattitatum (1) of the vulva. In contrast, the external gen- Pteropus hypomelanus (2) italia of noctilionids, mormoopids, phyllos- Pteropus neohibernicus (3) tomids, thyropterids, and natalids are dra- Pteropus temmincki (1) Dobsonia moluccesis (2) matically modified (see also, Wood Jones, '17; Dobsonia praedatrix (2) Wimsatt and Enders, '80). These bat fami- Epomorphorine-section lies show an elongation of the vulva in an Epomops franqueti (3) anteroposterior direction, an elongate cli- Hypsignathus monstrosus (2) Micropteropus pusillus (4) toris, prominent labia minora, and poorly Cynopterine-section developed postanal-circumanal folds. The Cynopterus sphinx (6) anteroposterior development of the vulva Cynopterus horsfieldi (1) appears to be a derived feature within euth- Balwnycteris maculata (2) Nyctimene albiventer (5) erian mammals, a similar evolutionary trend Nyctimene vizcaccia (1) being found only in the primates. Subfamily Macroglossinae Eonycteris spelaea (6) Ovarian morphology Megaloglossus woermanni (8) Macroglossus minimus (24) The ovaries of pteropodids are either Macroglossus sobrinus (3) spherical or slightly elongate and their his- Syconycteris australis (1) tology is typical of that of other mammals. Melonycteris melanops (6) Notopteris macdonaldi (3) In all pteropodids examined, both ovaries contain a variety of follicular types and are Wos. in parentheses represent sample sizes. equally functional, with ovulation alternat- ing between sides. Extensive networks of bats is equivalent to that found in other bat blood vessels are found in the ovarian hilus, families and in eutherians generally. The the mesenteries supporting the oviduct, and free uterine horns are long in pteropodids the cranial end of the uterus in many of the and their ovaries lie more superior than those taxa examined. This histological arrange- of emballonurids, rhinolophids, vesperti- ment allows for direct vascular (veno-arte- lionids, molossids, and phyllostomoids. The rial) shunts between these organs. Such a pteropodid arrangement is similar to that system occurs in Pteropus giganteus and its found in eutherians that also possess prim- vascular shunts mediate asymmetrical ovi- itive (duplex) uterine morphologies (Der- ductal and uterine reactions (Marshall, '49; moptera, Rodentia; Mossman, '77). '53). Although the present study was not de- A major dichotomy in female external signed to investigate questions of reproduc- genitalia exists between Megachiroptera and tive function, histological features of ovar- some families of Microchiroptera. In ptero- ian anatomy suggest that vascular shunts podids, the urogenital orifice is a transverse occur in a wide variety of pteropodid taxa. opening found immediately anterior to the The anatomical relationship of the ovary anus. A raised structure, the genital tuber- to the oviduct and uterus in pteropodids has cle, is directed caudally over the opening and no unusual features compared to those of contains a broad, flattened clitoris. The mar- other mammals. In all pteropodids exam- gins of the urogenital orifice are not raised ined, the ovary and oviduct are enveloped to form labia majora, but postanal and cir- by an ovarian bursa that is composed of a cumanal folds of unknown homology are pre- mesovarium and mesosalphinx. Phyllosto- sent. Pteropodid external genitalia are re- moid bats demonstrate a tremendous
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