Marmosa Gray, 1821

Voss, RS & Jansa, SA, 2009, Phylogenetic Relationships And Classification Of Didelphid Marsupials, An Extant Radiation Of New World Metatherian Mammals, Bulletin of the American Museum of Natural History 2009 (322), pp. 1-177 : 101-105

Marmosa Gray, 1821 Figure 41

CONTENTS: We recognize two subgenera, Marmosa Gray, 1821 , and Micoureus Lesson, 1842 (see Remarks, below).

The subgenus Marmosa contains andersoni Pine, 1972 ; lepida Thomas, 1888 (including

25 In fact, it has been suggested that they are not: ‘‘Considero que Thylatheridium es un género derivado, en el Plioceno inferior, de una de las especies de Monodelphis que, ante posibilidades ecológicas favorables, aceleró su ritmo evolutivo, apartándose rápidamente de sus congéneres de evolución lenta …’’ ( Reig, 1958: 90).

grandis Tate, 1931); mexicana Merriam, 1897 (including mayensis Osgood, 1913; savannarum Goldman, 1917; and zeledoni Goldman, 1917); murina Linnaeus, 1758 (including bombascarae Anthony, 1922; chloe Thomas, 1907; dorsigera Linnaeus, 1758; duidae Tate, 1931; guianensis Kerr, 1792; klagesi J.A. Allen, 1900; macrotarsus Wagner, 1842; madeirensis Cabrera,. 1913; maranii Thomas, 1924; meridionalis Miranda-Ribeiro, 1936; moreirae Miranda-Ribeiro, 1936; muscula Cabanis, 1848; parata Thomas, 1911; roraimae Tate, 1931; tobagi Thomas, 1911; and waterhousei Tomes, 1860); quichua Thomas, 1899 (including musicola Osgood, 1913); robinsoni Bangs, 1898 (including casta Thomas, 1911; chapmani J.A. Allen, 1900; fulviventer Bangs, 1901; grenadae Thomas, 1911; isthmica Goldman, 1912; luridavolta Goodwin, 1961; mimetra Thomas, 1921; mitis Bangs, 1898; nesaea Thomas, 1911; pallidiventris Osgood, 1912; ruatanica Goldman, 1911; and simonsi Thomas, 1899); rubra Tate, 1931 ; tyleriana Tate, 1931 (including phelpsi Tate, 1939); and xerophila Handley and Gordon, 1979 .

The subgenus Micoureus contains alstoni J.A. Allen, 1900 (including nicaraguae Thomas, 1905); constantiae Thomas, 1904 (including budini Thomas, 1920); demerarae Thomas, 1905 (including areniticola Tate, 1931; domina Thomas, 1920; esmeraldae Tate, 1931; limae Thomas, 1920; and meridae Tate, 1931); paraguayana Tate, 1931 (including cinerea Temminck, 1824 [preoccupied]); phaea Thomas, 1899 (including perplexa Anthony, 1922); and regina Thomas, 1898 (including germana Thomas, 1904; mapiriensis Tate, 1931 ; parda Tate, 1931; rapposa Thomas, 1899; and rutteri Thomas, 1924).

MORPHOLOGICAL DESCRIPTION: Combined length of adult head and body ca. 100– 210 mm; adult weight ca. 20–170 g. Rhinarium with two ventrolateral grooves on each side of median sulcus; dark circumocular mask present; pale supraocular spot absent; dark midrostral stripe absent; throat gland absent in some species (e.g., M. murina ) but present in adult males of other species (e.g., M. mexicana ). Dorsal pelage unpatterned, superficially brownish, reddish, or grayish, but dorsal hair bases always dark gray; dorsal guard hairs short and inconspicuous; ventral fur superficially whitish, yellowish, or orange, wholly or partly gray based (apparently never completely self-colored). Manus paraxonic (dIII 5 dIV); manual claws about as long as or slightly longer than fleshy apical pads of digits; dermatoglyph-bearing manual plantar pads present; central palmar epithelium smooth or sparsely covered with flattened tubercles (never densely tuberculate); carpal tubercles completely absent in some species (e.g., M. murina ), or only lateral carpal tubercles present in adult males (e.g., in M. lepida ), or both medial and lateral carpal tubercles present in adult males (e.g., in M. robinsoni ). Pedal digits unwebbed; dIV longer than other pedal digits; plantar surface of heel macroscopically naked, but all or part of heel covered with microscopic hairs in some species (e.g., M. rubra ). Pouch absent; mammae 3–1–3 5 7 (e.g., in M. lepida ) to 7– 1–7 5 15 (in M. mexicana ), all abdominalinguinal; cloaca present. Tail always substantially longer than combined length of head and body; slender and muscular (not incrassate); without a conspicuously furred base in some species (e.g., M. murina ) or tail base conspicuously furred to about the same extent dorsally as ventrally (e.g., in M. paraguayana ); naked caudal integument unicolored (all dark) in most species but mottled distally with white spots and/or white tipped in others (e.g., M. paraguayana ); caudal scales in spiral series (e.g., in M. murina ) or in both spiral and annular series (e.g., in M. mexicana ), each scale usually with three subequal bristlelike hairs emerging from distal margin; ventral caudal surface always modified for prehension distally, with apical pad bearing dermatoglyphs.

Premaxillary rostral process present in most species (absent in M. xerophila ). Nasals long, extending anteriorly beyond I1 (concealing nasal orifice in dorsal view), and conspicuously widened posteriorly near maxillaryfrontal suture. Maxillary turbinals elaborately branched. Lacrimal foramina usually two on each side, exposed to lateral view on or near anterior orbital margin. Supraorbital margins with distinct beads or prominent crests; flattened, triangular postorbital processes usually present in fully mature adults but substantially larger in some species than in others (absent or indistinct in M. rubra ). Left and right frontals and parietals separat- ed by persistent median sutures. Parietal and alisphenoid in contact on lateral braincase (no frontal-squamosal contact). Sagittal crest never developed. Petrosal usually not exposed laterally through fenestra in parietalsquamosal suture (fenestra absent).26 Parietalmastoid contact present (interparietal does not contact squamosal).

Maxillopalatine fenestrae present; palatine fenestrae absent in most species (but consistently present in some; e.g., M. mexicana ); maxillary fenestrae absent; posterolateral palatal foramina small, never extending anteriorly between M4 protocones; posterior palatal morphology conforms to Didelphis morphotype (with well-developed lateral corners, the choanae constricted behind). Maxillary and alisphenoid not in contact on floor of orbit (separated by palatine). Transverse canal foramen present. Alisphenoid tympanic process smoothly globular, without anteromedial process or posteromedial lamina enclosing the maxillary nerve (secondary foramen ovale usually absent),27 and not in contact with rostral tympanic process of petrosal. Anterior limb of ectotympanic suspended directly from basicranium. Stapes usually triangular, with large obturator foramen (microperforate and imperforate stapes occur as rare variants in several species). Fenestra cochleae exposed in most species, but fenestra concealed in sinus formed by caudal and rostral tympanic processes of petrosal in M. rubra . Paroccipital process small, rounded, adnate to petrosal. Dorsal margin of foramen magnum bordered by supraoccipital and exoccipitals, incisura occipitalis present.

Two mental foramina usually present on lateral surface of each hemimandible (one foramen or three foramina occur as rare,

26 We observed a fenestra between the squamosal and parietal on just two skulls, both of which are examples of Marmosa lepida . This trait occurs bilaterally on MNHN 1998-306 (from French Guiana) and unilaterally on MVZ 155245 (from Peru). All of the other six specimens of M. lepida that we examined for this character resemble other Marmosa spp. in lacking these openings.

27 Two out of 12 examined specimens of Marmosa regina have secondary foramina ovales formed by posteromedial bullar laminae: this trait occurs bilaterally on MVZ 190326 and unilaterally on MVZ 190328.

usually unilateral variants in some species); angular process acute and strongly inflected.

Unworn crowns of I2–I5 symmetrically rhomboidal (‘‘premolariform’’), with subequal anterior and posterior cutting edges, and increasing in length (mesiodistal dimension) from I2 to I5. Upper canine (C1) alveolus in premaxillary-maxillary suture; C1 simple (without accessory cusps in most species) or with posterior accessory cusp only (in M. lepida ). First upper premolar (P1) smaller than posterior premolars but well formed and not vestigial; second and third upper premolars (P2 and P3) subequal in height; P3 with posterior cutting edge only; upper milk premolar (dP3) large and molariform. Molars moderately carnassialized (postmetacristae are visibly longer than postprotocristae); relative widths usually M1, M2, M3, M4; centrocrista strongly inflected labially on M1–M3; ectoflexus indistinct or absent on M1, shallow but usually distinct on M2, and consistently deep on M3; anterolabial cingulum continuous with preprotocrista (complete anterior cingulum present) on M3. Last upper tooth to erupt is P3.

Lower incisors (i1–i4) with distinct lingual cusps. Unworn lower canine (c1) usually semiprocumbent, with flattened bladelike apex, with or without distinct posterior accessory cusp. Second lower premolar (p2) taller than p3; lower milk premolar (dp3) trigonid incomplete (bicuspid). Hypoconid labially salient on m3; hypoconulid twinned with entoconid on m1–m3; entoconid much taller than hypoconulid on m1–m3.

DISTRIBUTION: Species of Marmosa collectively range from the Mexican state of Tamaulipas southward throughout most of Central and tropical South America to Bolivia, Paraguay, and northern Argentina ( Hall, 1981; Creighton and Gardner, 2008b; Gardner and Creighton, 2008b). Although most species inhabit lowland rainforests, a few are restricted to dry habitats (e.g., M. xerophila ; Handley and Gordon, 1979) and some species of the subgenus Micoureus occur in montane rainforest at elevations in excess of 2000 m (e.g., M. mapiriensis sensu Tate, 1933: 76 ).

REMARKS: The monophyly of Marmosa (including Micoureus ) is supported by sequence data from five genes analyzed sepa- rately (figs. 28–32), in tandem (fig. 33), and in combination with nonmolecular characters (figs. 35, 36); generic monophyly is also supported by a uniquely shared insertion at the BRCA1 locus (fig. 31). Only a single morphological character, the possession of a rostral process of the premaxillae, optimizes as an unambiguous generic synapomorphy (appendix 5), but even this weak phenotypic evidence is compromised by the absence of a rostral process in M. xerophila , a species that we did not score for this study.

No published phylogenetic analysis supports the reciprocal monophyly of Marmosa and Micoureus , both of which have been treated as valid genera by recent authors (e.g., Gardner, 2005; Creighton and Gardner, 2008b; Gardner and Creighton, 2008b). Instead, species of Micoureus have consistently been recovered as nested within a paraphyletic group of Marmosa species ( Kirsch and Palma, 1995; Voss and Jansa, 2003; Jansa and Voss, 2005; Steiner et al., 2005; Jansa et al., 2006; Gruber et al., 2007). Obviously, there are several alternative taxonomic solutions to this problem.

One solution would be to treat Micoureus as a junior synonym of Marmosa without recognizing any subgenera of the latter. Another would be to recognize Micoureus as a subgenus of Marmosa and to name new subgenera for other monophyletic clusters of Marmosa species. A third would be to recognize Micoureus as a genus and to describe new genera as needed to make Marmosa monophyletic. Unfortunately, the first option would result in the loss of a useful name ( Micoureus , see below), whereas the second and third options are not currently workable because many species of Marmosa have not been included in any phylogenetic analysis, and their relationships are correspondingly obscure. Our interim solution is to move the currently intractable problem of paraphyly from the generic to the subgeneric level. Although taxonomic rank is biologically arbitrary, it affects binomial usage, which should be conformable with phylogenetic relationships insofar as these are known. In effect, because the use of generic names is obligatory under the current Linnaean system, it is crucial that genera be monophyletic.

The monophyly of Micoureus has been supported in every sequencing study to date that has included two or more exemplar species (e.g., Patton et al., 1996; Voss and Jansa, 2003; this study), and it may often be appropriate to indicate this fact in contradistinction to the paraphyly of the subgenus Marmosa . Where appropriate, this can be achieved using double quotes for the latter, as for the species Marmosa (‘‘ Marmosa ’’) lepida as contrasted with Marmosa (Micoureus) demerarae . Predictably, the subgeneric classification of Marmosa will be refined as future studies based on denser taxon sampling yield increasingly resolved estimates of relationships within this speciose group.

Most of the species herein referred to Marmosa have not been revised since Tate (1933), and some currently recognized synonymies are the result of uncritical lumping by subsequent authors (e.g., Hershkovitz, 1951; Cabrera, 1958). Recent analyses of both mtDNA sequence data (e.g., by Patton et al., 2000; Patton and Costa, 2003) and morphological characters ( Rossi, 2005) suggest that several nominal taxa currently listed as synonyms (e.g., of M. demerarae , M. murina , and M. robinsoni ) are probably valid species. Therefore, significant changes to the species-level taxonomy of Marmosa should be expected soon.