Diversidade de espécies no complexo Monodelphis brevicaudata (Didelphimorphia:Didelphidae), inferida por dados moleculares e morfológicos

Short‐tailed opossums of the Monodelphis revicaudata complex inhabit northern South America, and comprise three described species ‐ M. brevicaudata, M. glirina, and M. palliolata ‐ and two undescribed forms already recognized in prior studies. Species delimitation based solely on morphological features is difficult, and because of that many nominal taxa have been associated with this species complex, and several taxonomic arrangements have been proposed. Previous molecular phylogenetic studies using specimens of this species complex revealed substantial genetic divergence rates. The present study aims to elucidate the systematics of the M. brevicaudata species complex through the analyses of molecular and morphological characters. We performed phylogenetic analyses on two mitochondrial genes (cyt b and 16S), studied the external and cranial morphology, and investigated whether observed genetic variation is congruent with morphological differences. Our morphological results were generally concordant with the molecular results. We recognize nine species in the species complex. M. brevicaudata, M. palliolata, and M. glirina are considered valid species; M. touan is re‐established from the synonymy of M. brevicaudata and two new species are described and named; the species M. domestica proved to be closely related to specimens of the M. brevicaudata complex, and thus are considered as part of that group; we also recognized two new species without formallly naming them; M. maraxina is considered a synonym of M. glirina. Sexual dimorphism is observed in the species, and in two species males showed skulls significantly larger than females. Major rivers seem to have played an important role in generating genetic differentiation and phylogeographical structure of the species. The phylogeographical pattern suggests at least two diversification centers for the group, one in the Guiana shield, comprising species ranging north of the Amazon river, and another in the Brazilian shield, comprising M. glirina and M. domestica.O complexo de espécies M. brevicaudata possui distribuição reconhecida para o Norte da América do sul e compreende três espécies descritas ‐ M. brevicaudata, M. glirina, e M. palliolata ‐ e duas não descritas, reconhecidas em estudos prévios. A delimitação de espécies baseada somente em caracteres morfológicos é complicada, de forma que diversos táxons nominais já foram associados ao grupo e diversos arranjos taxonômicos foram propostos. Os poucos estudos baseados em dados moleculares que incluíram espécimes do complexo brevicaudata revelaram altas taxas de divergência genética. Este trabalho buscou elucidar a sistemática do complexo de espécies M. brevicaudata através do estudo dos padrões de variação morfológica e genética. Para tal, desenvolvemos análises filogenéticas baseadas em dois genes mitocondriais: citocromo b e 16 S rDNA. Adicionalmente, estudamos a morfologia externa e craniana dos espécimes, investigando a existência de congruência entre a variação genética e morfológica. As análises morfológicas foram, em geral, congruentes com as moleculares, as quais indicaram os mesmos clados em todas as análises filogenéticas. Foram formalmente reconhecidas nove espécies para o complexo. Monodelphis brevicaudata, M. palliolata e M. glirina são consideradas espécies válidas; M. touan é revalidado da sinonímia de M. brevicaudata e duas espécies novas são descritas e nomeadas; a espécie M. domestica provou ser intimamente relacionada a espécimes do grupo brevicaudata, sendo aqui considerada como integrante do referido grupo; duas espécies reconhecidas como distintas permanecem sem uma descrição formal; M. maraxina é sinonimizada com M. glirina. Foi observado dimorfismo sexual para as espécies estudadas, sendo que para as duas espécies estatisticamente testadas (teste T de student), M. glirina e M. sp. nov. “Trombetas”, os machos apresentaram crânios significativamente maiores que as fêmeas. Rios de grande porte parecem ter participado na diferenciação genética e estruturação filogeográfica das espécies. O padrão filogeográfico encontrado sugere ao menos dois centros de diversificação para o grupo, um no escudo das Guianas, envolvendo as espécies ao norte do rio Amazonas, e outro no escudo brasileiro, envolvendo M. glirina e M. domestica

Monodelphis glirina

MONODELPHIS GLIRINA (WAGNER, 1842) Type information: Holotype not cited in original description. Type locality ‘Mamoré’, Rondônia, Brazil. ‘Rio Mamoré, Cachoeira da Pau grande’ according to Pelzeln (1883), 10 ° 28′S, 65 ° 24′W (Vanzolini, 1993). Collected by Johann Natterer. The type specimen is possibly at the Naturhistorisches Museum Wien (NMW), where part of Natterer’s collection can be found. Synonyms: Didelphys glirina Wagner, 1842. Morphological diagnosis: Same as for the M. brevicaudata complex with the following additions: HBL averages 137 mm in adult females and 153 mm in adult males (Supporting Information Table S2). Dorsal pelage with grizzled, light grey coloured stripe at mid-dorsum, differing from the light orange to orange sides (Fig. 4); head pelage orange laterally and greyish dorsally, with the mid-dorsal stripe broad, occupying all crown of the head between the eyes; underparts greyish cream to greyish light-orange, not sharply differentiated from the orange sides (Fig. 4); throat commonly slightly more washed with orange than the rest of the venter; mammae at the inguinal/ abdominal region, one central and eight distributed circumferentially around it (MPEG 1318, 10134, 38985, 39115, 39140); tail covered with body fur to about the same extent above and below, up to one sixth of the caudal length. CBL averages 36.5 mm in adult females and 39.4 mm in adult males (Supporting Information Table S2); interorbital region relatively narrow (Fig. 5); zygomatic arches slightly rounded anteriorly; maxillopalatine foramina relatively long (Fig. 5); UMS averages 8.1 mm in adult females and 8.2 mm in adult males (Supporting Information Table S2). Geographical distribution: South-eastern Peru, northern Bolivia and Brazil in the states of Acre, Rondônia, southern Amazonas, northern Mato Grosso, and Pará south of the Amazon river, including the eastern margin of the Xingu river (Fig. 6). Monodelphis glirina occurs in sympatry with M. touan in southeastern Pará (see the Geographical distribution section of M. touan above for details). Geographical variation: Monodelphis glirina exhibits high morphological variation, mainly in the body pelage colour. Specimens from east of the Xingu river (localities Canaã dos Carajás, Marabá, São Félix do Xingu, and São João do Araguaia, in the state of Pará) lack the mid-dorsal stripe. Instead, they exhibit upperparts greyish, with lateral orange fur restricted either to the contact line between anterior body sides and venter or to head sides. Whereas specimens of M. glirina from west of the Xingu river have greyish yellow ventral pelage, with grey-based and yellowishtipped hairs, specimens from Marabá, on the opposite side of the Xingu river, exhibit notably darker ventral fur (grey coloured). Another specimen from east of the Xingu river (MPEG 10134, São João do Araguaia) shares with other specimens from this region the absence of a distinct stripe at mid-dorsum, but exhibits brownish orange (instead of greyish) upper fur, and greyish light-orange underparts. Amongst specimens from west of the Xingu river, which show orange body sides, the ones from the state of Mato Grosso are generally more greyish and paler, with the grey mid-dorsal stripe appearing wider, and the orange portion on body sides proportionally lighter and narrower, restricted to the area adjacent to the venter (but not so restricted as in specimens from east of the Xingu river). In many specimens the orange fur of the body sides becomes gradually narrower toward the back, with posterior part of the body grey coloured instead of orange. The venter is yellowish, with hairs grey at the base. By contrast, specimens from Altamira, Itaituba, and Santarém, in the state of Pará, are brighter orange on the flanks, with the mid-dorsal stripe generally narrower and well delimited. The venter is more washed with orange than in specimens from Mato Grosso. Specimens from Santa Rosa, Bolivia, resemble those from Altamira, Itaituba, and Santarém with respect to dorsal and lateral pelage, but show more greyish ventral pelage. Remarks: In this study, we analysed some specimens from the eastern margin of the Xingu river labelled as M. domestica (precisely from Marabá and São Félix do Xingu). Morphological traits of their skulls revealed more similarities to M. glirina than to M. domestica. The inclusion of specimens from Marabá in our molecular analysis allowed us to confirm their allocation to M. glirina, and to extend the geographical distribution of M. glirina to the eastern bank of the Xingu river. We concluded that the two specimens from São Félix do Xingu (MPEG 1318 and MZUSP 9931) are the specimens cited by Carvalho (1960) as Monodelphis brevicaudata emiliae. Pine & Handley presumed M. b. emiliae from Carvalho (1960) to be their Monodelphis species ‘D’. However, our analyses have shown that M. b. emiliae as recognized by Carvalho (1960) is actually M. glirina.Published as part of Pavan, Silvia Eliza, Rossi, Rogerio Vieira & Schneider, Horacio, 2012, Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species, pp. 190-223 in Zoological Journal of the Linnean Society 165 (1) on pages 202-203, DOI: 10.1111/j.1096-3642.2011.00791.x, http://zenodo.org/record/540729

Monodelphis touan

<i>MONODELPHIS TOUAN</i> (SHAW, 1800) <p> <i>Type information:</i> Holotype lost, from ‘Cayenne’, French Guiana. Neotype FMNH 21720, designated by Voss <i>et al</i>. (2001), an adult male from Cayenne, 04 ° 56′N, 52 ° 20′W (Gardner, 2008) preserved as skin and skull. Collected by S. Klages on 26.ii.1917.</p> <p> <i>Synonyms:</i> <i>Viverra Touan</i> Shaw, 1800; <i>Mustela touan</i> Bechstein, 1800; <i>Mustela touan</i> Daudin in Lacépède, 1802; <i>Didelphis tricolor</i> Geoffroy, 1803.</p> <p> <i>Morphological diagnosis:</i> Same as for the <i>M. brevicaudata</i> complex with the following additions: HBL averages 137 mm in adult females and 159 mm in adult males (Supporting Information Table S2). Dorsal pelage with grizzled, grey coloured stripe at mid-dorsum, contrasting with reddish sides (Fig. 4); head pelage reddish laterally, with mid-dorsal stripe narrow, sometimes ill-defined, confined by a band of red hairs above each eye; underparts greyish cream, sharply differentiated from the reddish sides (Fig. 4); throat and chin distinctly reddish; tail dorsally covered with body fur to about one third of the caudal length; ventrally, body fur coverage is limited to the tail’s connection with the body. CBL averages 35.5 mm in adult females and 39.8 mm in adult males; interorbital region relatively narrow (Fig. 5); zygomatic arches slightly convergent anteriorly; maxillopalatine foramina relatively short (Fig. 5); UMS averages 7.8 mm in adult females and 8.0 mm in adult males (Supporting Information Table S2).</p> <p> <i>Geographical distribution:</i> North-eastern South America, from French Guiana and the Brazilian state of Amapá southward to the Brazilian state of Pará south of the Amazon river and east of the Xingu river, including Marajó Island (Fig. 6). Specimens of <i>M. touan</i> from south of the Amazon river were found in sympatry with specimens of <i>M. glirina</i> in the municipality of Marabá, in south-eastern Pará. Both species were caught in the same line of pitfall traps at Serra dos Carajás (A. C. M. Oliveira, UFPA – Universidade Federal do Pará, Belém, Brazil, pers. comm.), indicating syntopy for them.</p> <p> <i>Geographical variation:</i> Specimens from localities south of the Amazon river are effectively distinguished from specimens from north of the Amazon river by exhibiting broader mid-dorsal stripe on head, coverage of the tail by body fur extending only about one fifth (in contrast to one third or one half) of caudal length, darker colour of tail (the portion not covered by body pelage), ears, and feet. Cranially, when comparing individuals from the same sex and age class, specimens from south exhibit larger molars, larger bulla, and slightly broader braincase and nasals.</p> <p>Amongst specimens from the north of the Amazon river, the extension of body fur on the dorsal surface of the tail corresponds to about one third of caudal length in specimens from Amapá, and to about one half of caudal length in specimens from French Guiana. Specimens from Amapá also have skulls slightly longer when compared to French Guianan specimens, which show proportionally broader skulls.</p> <p> <i>Remarks:</i> Based on Buffon’s (1789) description of <i>Le Touan</i>, with type locality in Cayenne, French Guiana, Shaw (1800) described <i>Viverra touan</i>. Shaw noted a blackish dorsal fur, ferrugineous sides and white lower parts, being the first reference to a tricoloured specimen of the <i>M. brevicaudata</i> group. <i>Mustela touan</i> Bechstein, 1800 and <i>Mustela touan</i> Daudin in Lacépède, 1802 were also based on Buffon’s specimen, and are objective synonymies of <i>Viverra touan</i>. Geoffroy (1803) described <i>Didelphis tricolor</i> based also on a tricoloured specimen from Cayenne (MNHN 1990.421). Until now, <i>D. tricolor</i> has been regarded as a synonym of <i>M. brevicaudata</i> (e.g. Thomas, 1888; Cabrera, 1919; Gardner, 2005; Pine & Handley, 2008). Our new taxonomic arrangement, however, implies that <i>D. tricolor</i> should be considered as a synonym of <i>M. touan</i>.</p> <p> The association of the name <i>M. touan</i> to the specimens from the eastern clade of our molecular analyses is explained by the morphological similarity of the neotype of <i>V. touan</i> Shaw, 1800 (FMNH 21720) with those specimens. Our genetic samples of this clade include specimens from Cayenne, the type locality of the nominal taxa. The resurrection of <i>M. touan</i> to include the eastern clade is supported by the monophyly and genetic distinctiveness of this group, allied to a morphological differentiation from the species <i>M. brevicaudata</i> (<i>sensu stricto</i>).</p> <p> Amongst the haplotypes of the eastern clade, the ones from the Brazilian state of Pará (localities south of the Amazon river) were regarded as <i>Monodelphis</i> species ‘D’ by Pine & Handley (2008). These specimens are morphologically distinct from specimens from the north of the Amazon river (see the Geographical variation section above), and form a strongly supported, truly monophyletic lineage that is embedded amongst haplotypes from French Guiana and the state of Amapá, Brazil (north of the Amazon river) in most analyses, rendering a paraphyletic group of northern specimens in most analyses (Fig. 2). However, the monophyly of the northern specimens was also recovered in some analyses. Faced with the absence of resolution in our molecular analyses, we took a conservative decision, considering <i>M</i>. species ‘D’ under <i>M. touan</i> as a geographical variant of the latter, instead of describing it as a new species.</p>Published as part of <i>Pavan, Silvia Eliza, Rossi, Rogerio Vieira & Schneider, Horacio, 2012, Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species, pp. 190-223 in Zoological Journal of the Linnean Society 165 (1)</i> on pages 201-202, DOI: 10.1111/j.1096-3642.2011.00791.x, <a href="http://zenodo.org/record/5407298">http://zenodo.org/record/5407298</a&gt

Monodelphis maraxina Thomas 1923

MONODELPHIS MARAXINA THOMAS, 1923 Monodelphis maraxina Thomas, 1923 was described for Marajó Island, in eastern state of Pará. Thomas (1923) suggested that M. maraxina is closely related to M. domestica. Subsequent authors agreed with him, some of which even regarded M. maraxina as a synonym of M. domestica (e.g. Cabrera, 1958; Emmons & Feer, 1990, 1997). However, Pine (1980) suggested that a relationship of M. maraxina with members of the M. brevicaudata group would be more reasonable on zoogeographical grounds. He also noted that the relative hairlessness of the tail and the buffy coloration of body sides are conditions shared with specimens of M. brevicaudata from the east bank of the Tapajós river (= M. glirina). Recently, based on Pine’s (1980) view, Solari (2010) included M. maraxina in the M. brevicaudata group. Our morphological analysis of the holotype of M. maraxina (BMNH 12.5.11.13) through photographs led us to conclude that this form undoubtedly belongs to the M. brevicaudata complex. The colour pattern observed in specimens of M. glirina from the east bank of the Xingu river shows a striking concordance with the original description of M. maraxina, and our analysis confirmed that these two forms have highly similar skin and skulls. Similarities between the faunas of the Marajó Island and the adjacent area at the eastern margin of the Xingu river are expected, as indicated by other vertebrate groups (e.g. Nascimento et al., 1991; Avila-Pires, 1995; Fernandes, Cardoso da Silva & Silva Jr, 1995; Ron, 2000). Furthermore, our recent field work at Marajó uncovered specimens of another species of the M. brevicaudata complex that is also present on the east bank of the Xingu river (M. touan), confirming that these areas are able to share species of short-tailed opossum. Given the substantial morphological similarity between the holotype of M. maraxina and specimens of M. glirina from east of the Xingu river, and the evidence that these areas are able to share species of short-tailed opossum, we argue that M. maraxina may represent a geographical variant of M. glirina. However, as we have not performed molecular and direct morphological analyses of specimens regarded as M. maraxina, and because our general analyses are not conclusive with respect to M. glirina, which may represent a complex of species rather than an unique species, more accurate analyses are needed to answer this question. At this time, we maintain M. maraxina as a valid species included in the M. brevicaudata complex.Published as part of Pavan, Silvia Eliza, Rossi, Rogerio Vieira & Schneider, Horacio, 2012, Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species, pp. 190-223 in Zoological Journal of the Linnean Society 165 (1) on pages 210-211, DOI: 10.1111/j.1096-3642.2011.00791.x, http://zenodo.org/record/540729

Data from: Rate of evolutionary change in cranial morphology of the marsupial genus Monodelphis is constrained by the availability of additive genetic variation

We tested the hypothesis that the rate of marsupial cranial evolution is dependent on the distribution of genetic variation in multivariate space. To do so, we carried out a genetic analysis of cranial morphological variation in laboratory strains of Monodelphis domestica and used estimates of genetic covariation to analyze the morphological diversification of the Monodelphis brevicaudata species group. We found that within-species genetic variation is concentrated in only a few axes of the morphospace and that this strong genetic covariation influenced the rate of morphological diversification of the brevicaudata group, with between-species divergence occurring fastest when occurring along the genetic line of least resistance. Accounting for the geometric distribution of genetic variation also increased our ability to detect the selective regimen underlying species diversification, with several instances of selection only being detected when genetic covariances were taken into account. Therefore, this work directly links patterns of genetic covariation among traits to macroevolutionary patterns of morphological divergence. Our findings also suggest that the limited distribution of Monodelphis species in morphospace is the result of a complex interplay between the limited dimensionality of available genetic variation and strong stabilizing selection along two major axes of genetic variation

Posterior_and_matrices_Gnoise

BSFG model priors and posterior distributions, when estimating G based on random noise. File names follow the convention established by the BSFG model (Runcie & Mukherjee, 2013)

Species_and_node_information

Information on species' trait means and branch lengths used when estimating rate of morphological evolution. Branch names correspond to the names reported in the main text

Matrices

Variance/covariance matrices used in this study, separated by species. The BSFG G-matrix is named G_Bayes. The BSFG P-matrix is named P_Bayes

Priors_Posterior_and_Measurements

BSFG model input data and resulting posterior distributions. File names follow the convention established by the BSFG model (Runcie & Mukherjee, 2013). A file containing the 30 linear measurements collected in the skull of each strain specimen is also attached