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Old World Fruitbat Phylogeny: Evidence for Convergent Evolution and an Endemic African Clade (Megachiroptera͞12s Rrna͞valine Trna͞convergence͞biogeography)

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Old World Fruitbat Phylogeny: Evidence for Convergent Evolution and an Endemic African Clade (Megachiroptera͞12s Rrna͞valine Trna͞convergence͞biogeography) Proc. Natl. Acad. Sci. USA Vol. 94, pp. 5716–5721, May 1997 Evolution Old World fruitbat phylogeny: Evidence for convergent evolution and an endemic African clade (megachiropteray12S rRNAyvaline tRNAyconvergenceybiogeography) LAURA J. HOLLAR AND MARK S. SPRINGER Department of Biology, University of California, Riverside, CA 92521 Communicated by Charles G. Sibley, Retired, Santa Rosa, CA, March 18, 1997 (received for review November 12, 1996) ABSTRACT Knud Andersen (1912, Catalogue of the Chi- roptera in the Collections of the British Museum: I. Megachirop- tera, British Museum of Natural History, London) divided Old World fruitbats (family Pteropodidae) into the rousettine, cynopterine, epomophorine, eonycterine, and notopterine sec- tions. The latter two sections comprise the subfamily Macro- glossinae; members of this subfamily exhibit specializations for nectarivory (e.g., elongated, protrusible, brushy tongues) and cluster together in cladistic analyses based on anatomical characters. Other evidence, including single-copy DNA hy- bridization, suggests that macroglossines are either paraphyl- etic or polyphyletic; this implies that adaptations for pollen and nectar feeding evolved independently in different macro- glossine lineages or were lost in nonmacroglossines after evolving in a more basal common ancestor. Hybridization data also contradict Andersen’s phylogeny in providing support for FIG. 1. Lateral views of the skulls and mandibles of (a) Rousettus an endemic African clade that includes representatives of aegyptiacus,(b)Pteralopex atrata,(c)Epomophorus gambianus,(d) three of Andersen’s sections. Here, we present complete Cynopterus sphinx,(e)Melonycteris melonops, and (f) Megaloglossus woermanni mitochondrial 12S rRNA and valine tRNA gene sequences for . Modified after Andersen (1). 20 pteropodids, including representatives of all of Andersen’s sections, and examine the aforementioned controversies. Max- the rousettines, Andersen judged Rousettus (Fig. 1a) as similar imum likelihood, minimum evolution, and maximum parsi- in morphology to the ancestor of all pteropodids (e.g., no mony analyses all contradict macroglossine monophyly and surface cusps on P4 and M1, no narrowing and degeneration of provide support for an African clade that associates Megalo- the cheekteeth, rostrum of moderate length). Rousettus has a glossus and Lissonycteris and those two with Epomophorus.In mixed diet that includes soft fruits andyor fruit juices as well conjunction with the DNA hybridization results, there are now as nectar (3, 4). Among other rousettines (Fig. 1b), Acerodon, independent lines of molecular evidence suggesting: (i) con- Pteralopex, and some species of Pteropus routinely deal with vergent evolution of specializations for nectarivory, at least in fruit pulp and have anatomical features consistent with these Megaloglossus versus other macroglossines, and (ii) a previ- dietary preferences (1), e.g., robust dentary with expanded ously unrecognized clade of endemic Africa taxa. Estimates of coronoid process and masseteric fossa. The Epomophorus divergence time based on 12S rRNA and DNA hybridization section contains genera that are African in distribution; mem- data are also in good agreement and suggest that extant bers of this section are characterized by a distinct flattening of fruitbats trace back to a common ancestor 25 million to 36 the braincase (Fig. 2c). Like Rousettus, many epomophorines million years ago. are mixed feeders (i.e., combination of frugivory and nec- tarivory) and have anatomical features (e.g., of the mandible) Knud Andersen’s monograph (1) remains the most compre- that are intermediate between Acerodon-Pteralopex and mac- hensive treatment of the Megachiroptera (Old World fruit- roglossines. The Cynopterus section (Fig. 1d) contains forms bats) even though several new genera (e.g., Aproteles, Paranyc- characterized by traits such as a short rostrum and a tendency timene) have been described (2, 3). Andersen included all to develop cusps on P4 and M1. Included in Andersen’s fruitbats in the family Pteropodidae with three subfamilies: a Cynopterus section is the aberrant Nyctimene, which is unique paraphyletic Pteropodinae, which contains the majority of among fruitbats with its partially insectivorous diet. Finally, the species and genera; the monotypic Harpyionycterinae; and the eonycterine and notopterine sections together comprise the presumed monophyletic subfamily Macroglossinae containing Macroglossinae. Macroglossines are unique among fruitbats in taxa with specializations for nectarivory. Andersen recognized having a more elongated, slender, protrusible tongue; further, the Macroglossinae as a sister-taxon to other living fruitbats. the tip and lateral area of the base of the tongue are covered Beyond his subfamilial distinctions, Andersen divided fruit- by long, filiform papillae that give the tongue a brushlike bats into five sections. Nonmacroglossines are placed in the appearance and function in extracting pollen from flowers (see rousettine, epomophorine, and cynopterine sections. Among Fig. 2). Osteological modifications in macroglossines include cheektooth reduction and degeneration, a narrower and more The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked ‘‘advertisement’’ in accordance with 18 U.S.C. §1734 solely to indicate this fact. Abbreviations: sc, single copy; mt, mitochondrial; Myr, million years; T-PTP, topology-dependent permutation tail probability. Copyright q 1997 by THE NATIONAL ACADEMY OF SCIENCES OF THE USA Data deposition: The sequences reported in this paper have been 0027-8424y97y945716-6$2.00y0 reported in the GenBank database (accession nos. U61077 and PNAS is available online at http:yywww.pnas.org. U93053– U93073). 5716 Downloaded by guest on September 28, 2021 Evolution: Hollar and Springer Proc. Natl. Acad. Sci. USA 94 (1997) 5717 (12). Sequence alignments were modified following secondary structure models (13–14). Regions where alignments were ambiguous were omitted from phylogenetic analyses. For 12S rRNA, we omitted the regions between 8 and 89, 10 and 109, 49 and 139, 17 and 189,189and 179,24andC9, 35 and 359,359 and 36 (except the last six bases), and 39P and 39P9[stem numbers follow Springer and Douzery (13)]; for tRNA valine, we omitted the dihydrouridine and ribothymidine loops. We also omitted sites with gaps. This resulted in 927 characters. Maximum likelihood, minimum evolution, and parsimony (uniform and differential weighting schemes) were used to estimate phylogenetic trees using the three microchiropterans as outgroups. These analyses, including topology-dependent permutation tail probability (T-PTP) tests (15), bootstrapping (16), and the Kishino–Hasegawa (17) test, were conducted with PAUP 4.0d49 and 4.0d52 for Power MacIntosh (18). Bootstrap and T-PTP tests included 500 replications except for the maximum-likelihood analysis with a gamma rate- distribution (100 replications). For the maximum likelihood FIG. 2. Diagrams of the superior surfaces of the tongues of (a) analyses, we used empirical base frequencies with full heuristic Macroglossus lagochilus,(b)Eonycteris spelaea, and (c) Cynopterus searches. The first analysis was based on the HKY85 (19) sphinx. Anterior filiform papillae are indicated as FP. Macroglossus model, which assumes a 2:1 transition:transversion ratio with and Eonycteris are macroglossines; Cynopterus is a cynopterine. Mod- equal rates among sites. The second analysis used a transi- ified after Andersen (1). tion:transversion ratio of 4.32 and a gamma distribution with recumbent coronoid process, and a lower mandibular condyle a shape parameter of 0.22. These parameters were estimated (Fig. 1 e and f). from the five equally most parsimonious trees following the A cladistic reanalysis of Andersen’s morphological data recommendation of Swofford et al. (20). Minimum-evolution confirms many of Andersen’s conclusions, including macro- (21) trees were estimated using Jukes and Cantor (22), glossine monophyly and, with a few exceptions, the monophyly Kimura-2 parameter (23), and Tamura and Nei (24)-corrected of the Cynopterus and Epomophorus sections (5). The Rouset- distances with full heuristic searches. For each distance cor- tus section is paraphyletic based on this reanalysis. Single-copy rection, we used both equal rate and gamma-rate distribution (sc) DNA hybridization (6), restriction fragment length poly- options. For the parsimony analyses, we used full heuristic morphism analysis (7), and an evaluation of female reproduc- searches with 10 random input orders. Initially, all characters tive characters (8) all suggest that macroglossines are paraphyl- were weighted equally. We also downweighted stem sites by etic or polyphyletic with the implication that nectarivorous 0.62 to account for nonindependence (11). Finally, we re- tongue characters evolved independently in different lineages weighted characters proportional to their consistency indices or were reversed once evolved in a common ancestor. scDNA until a stable topology was obtained. Character-state trans- hybridization also provides evidence for an African clade that formations were either unweighted or weighted to account for includes Megaloglossus, Lissonycteris, and Epomophorus. the transition-bias in animal mtDNA; in the latter case trans- Andersen included each of these genera in a separate section. versions were weighted more heavily than transitions in both Here, we
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