Species Limits and Phylogenetic Relationships in the Didelphid Marsupial Genus Thylamys Based on Mitochondrial Dna Sequences and Morphology
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SPECIES LIMITS AND PHYLOGENETIC RELATIONSHIPS IN THE DIDELPHID MARSUPIAL GENUS THYLAMYS BASED ON MITOCHONDRIAL DNA SEQUENCES AND MORPHOLOGY THOMAS C. GIARLA Department of Ecology, Evolution, and Behavior, and J.F. Bell Museum of Natural History University of Minnesota 1987 Upper Buford Circle, St. Paul, MN 55108 ROBERT S. VOSS Division of Vertebrate Zoology (Mammalogy) American Museum of Natural History SHARON A. JANSA Department of Ecology, Evolution, and Behavior, and J.F. Bell Museum of Natural History University of Minnesota 1987 Upper Buford Circle, St. Paul, MN 55108 BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY Number 346, 67 pp., 19 figures, 25 tables Issued December 16, 2010 Copyright E American Museum of Natural History 2010 ISSN 0003-0090 CONTENTS Abstract.......................................................... 3 Introduction . ...................................................... 3 Taxonomic History ................................................. 3 SpeciesRecognitionCriteria........................................... 4 MaterialsandMethods................................................ 5 MuseumCollections................................................ 5 Taxon Sampling ................................................... 5 DNA Extraction and Gene Sequencing ................................... 8 Phylogenetic Analyses .............................................. 10 Morphology..................................................... 11 MolecularResults................................................... 13 Sequence Characteristics ............................................ 13 Phylogenetic Analyses .............................................. 13 Morphological Character Variation . ................................... 27 External Characters................................................ 27 Craniodental Characters ............................................ 28 Taxonomy . ..................................................... 33 Xerodelphys, new subgenus .......................................... 34 Thylamys karimii (Petter, 1968) ....................................... 36 Thylamys velutinus (Wagner,1842)..................................... 37 Subgenus Thylamys Gray,1843....................................... 38 Thylamys macrurus (Olfers, 1818) . ................................... 38 Thylamys pusillus (Desmarest,1804).................................... 39 TheElegansGroup................................................ 44 Thylamys elegans (Waterhouse, 1839) ................................... 44 Thylamys pallidior (Thomas, 1902) . ................................... 46 Thylamys tatei (Handley,1957)....................................... 49 TheVenustusGroup............................................... 50 Thylamys sponsorius (Thomas,1921).................................... 51 Thylamys venustus (Thomas,1902)..................................... 56 Discussion . ..................................................... 58 Acknowledgments.................................................. 59 References........................................................ 61 Appendix1:GazetteerofSequencedSpecimens............................. 65 Appendix 2: Primers Used for Amplification of CYTB, COX2, and ND2 ........... 67 2 ABSTRACT Species of the didelphid marsupial genus Thylamys, commonly known as fat-tailed mouse opossums, are broadly distributed in the open habitats of central and southern South America. In this report we examine species limits in the genus and infer phylogenetic relationships among Thylamys species using both molecular phylogenetic and morphological methods. We assessed species limits using a broad geographic sample of DNA sequences from the mitochondrial gene cytochrome b in conjunction with morphological character analysis, and we inferred phylogenetic relationships among species using the cytochrome-b dataset in addition to sequences from the mitochondrial genes cytochrome c oxidase subunit II and NADH dehydrogenase 2 for a representative subset of individuals. Based on the results of these analyses, we recognize Xerodelphys (new subgenus) for T. karimii and T. velutinus,andwe recognize seven valid species in the nominotypical subgenus. The latter includes T. macrurus, T. pusillus, and two monophyletic species groups: the Elegans Group (T. elegans, T. pallidior, T. tatei) and the Venustus Group (T. sponsorius, T. venustus). Analysis of cytochrome-b sequences additionally reveals deep phylogeographic structuring in three species (T. pallidior, T. pusillus, T. venustus), each of which contains two or three robustly supported allopatric haplogroups. The existence of undescribed Peruvian forms of the Elegans Group is also plausibly indicated. We provide morphological diagnoses of all species recognized as valid in this report, summarize information about geographic distributions, comment on previous misidentifications, and briefly consider historical-biogeographic scenarios with a focus on dispersal events across the Andes. INTRODUCTION America, the systematics of this group are of considerable biogeographic interest. Unfor- Species of the didelphid marsupial genus tunately, neither the number of valid species Thylamys, commonly known as fat-tailed in the genus nor their evolutionary relation- mouse opossums, are widely distributed in ships has been convincingly resolved by savanna woodlands, thornscrub, semidesert previous studies. shrublands, shrubby steppe, montane thick- ets, and other more or less open, nonforest Taxonomic History habitats from western Peru and eastern Brazil southward to central Chile and Patagonia. Most of the nominal taxa now included in Their common English name refers to the Thylamys were referred to the ‘‘Elegans seasonal deposition of caudal fat (fig. 1), a Group’’ of Marmosa by Tate (1933), who phylogenetically derived trait that Thylamys recognized eight of them as valid species. shares with its sister taxon Lestodelphys (see Subsequent authors have recognized as few Morton, 1980). Together, Thylamys, Lesto- as one to as many as 10 species in this group, delphys, and four other didelphid genera which was first recognized as a valid genus in (Chacodelphys, Cryptonanus, Gracilinanus, its currently accepted sense by Gardner and Marmosops) comprise the tribe Thylamyini, Creighton (1989). Although the current one of two well-supported suprageneric classification (Creighton and Gardner, 2008) groups of small, mouselike or ‘‘murine’’ is based on an impressive number of recent opossums (Voss and Jansa, 2009). revisionary studies (Palma and Yates, 1998; Although the family Didelphidae is a Flores et al., 2000; Meynard et al., 2002; predominantly lowland rainforest clade, Thy- Palma et al., 2002; Solari, 2003; Braun et al., lamys is the most species-rich and widely 2005; Carmignotto and Monfort, 2006), no distributed of several opossum lineages that study to date has included material from all invaded nonforest habitats in the Miocene of the species now regarded as valid. (Jansa et al., in prep.). Because geographic Another notable aspect of most previous patterns of endemism and cladogenesis systematic analyses of Thylamys is an exclu- among fat-tailed mouse opossums are poten- sive reliance either on molecular or morpho- tially informative about the late Tertiary logical methods. Both approaches have history of nonforest environments in South unique advantages and limitations. Analyses 3 4 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY NO. 346 Fig. 1. Thylamys pallidior from Bahı´a Cracker (42u569S, 64u209W), Chubut, Argentina, photographed by Darı´o Podesta´ in January 2009. based on DNA sequencing, for example, morphological voucher material, and we have the advantage of abundant character assessed the taxonomic implications of our data, but sequence data can be difficult to results by comparing voucher material with interpret in the absence of phenotypic holotypes, neotypes, and other museum criteria linking gene trees to name-bearing specimens. types and other unsequenced material. Ad- ditionally, gene sequencing is relatively Species Recognition Criteria expensive, and the restricted availability of preserved tissue samples has hitherto limited Despite a plethora of published species molecular studies to treatments of no more definitions (reviewed by deQueiroz, 1998), than a few dozen individuals. By contrast, most evolutionary biologists agree that con- morphological analyses have the advantage temporaneous species should be genetically of almost cost-free data collection and independent lineages. For a number of abundant material, but they are often theoretical and practical reasons, mtDNA hindered by a poverty of taxonomically sequence monophyly and morphological informative characters. diagnosability are now routinely used as joint Herein we combine both approaches by criteria for species recognition by vertebrate analyzing .100 mitochondrial gene sequenc- systematists (Zamudio and Greene, 1997; es representing populations throughout the Frost et al., 1998; Patton et al., 2000; Wiens known distribution of Thylamys, including and Penkrot, 2002). Because substitution exemplars of all currently recognized species rates and haplotype coalescence are, in and most of the nominal taxa purported to be general, much more rapid for mitochondrial valid. We associated these sequence data with than for nuclear genes (Moore, 1995; Pa- phenotypic character variation by examining lumbi and Cipriano, 1998), mitochondrial 2010 GIARLA ET AL.: DIDELPHID MARSUPIAL GENUS THYLAMYS 5 sequence