October 23, 2021

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An integrative analysis uncovers a new, pseudo-cryptic species of Amazonian marmoset (Primates: Callitrichidae: Mico) from the arc of deforestation

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Morphology

All the marmosets from the Juruena–Teles Pires interfluve have discrete and objectively identifiable diagnostic states in pelage colour characters: the uniform lead coloration of saddle and rump and the cream-silvery underparts, which present orangish hues in living specimens (Fig. 2), are autapomorphies that readily distinguish these marmosets from M. emiliae and all other Mico species. The Juruena–Teles Pires marmosets, M. argentatus, M. emiliae, M. marcai, M. melanurus, and M. rondoni are clearly diagnosable in terms of pelage colour (Table 1; Fig. 3).

Phylogenomics

We obtained a molecular dataset consisting of 2081 loci spanning 717,129 base pairs, representing an average sampling effort at the DNA level of 22,410 base pairs per specimen (n = 32). After analyses in PartitionFinder2, the 2081 loci were clustered into 421 partitions. In both Bayesian inference and Maximum Likelihood phylogenetic analyses, species monophyly and species-level relationships were highly supported (pp ≥ 0.99; bp > 70%) with exception of M. emiliae, M. leucippe, and M. argentatus (Fig. 4; Supplementary Fig. S7). As expected, we retrieved four lineages or species groups in the genus Mico and found lineage membership patterns coherent with our predictions based on morphological synapomorphies. The Juruena–Teles Pires marmosets are monophyletic, sister to M. marcai, and both form a strongly supported lineage with M. melanurus. Mico emiliae is monophyletic, but nested within a clade that also includes paraphyletic M. leucippe and M. argentatus. These three species, together with M. intermedius, M. munduruku, and M. rondoni comprise the second major lineage of Mico (Fig. 5). A third lineage is comprised of M. humeralifer and M. mauesi, and Mico saterei was retrieved as an additional monotypic lineage. The clade formed by the Juruena–Teles Pires marmosets does not include M. emiliae specimens, nor is it sister to the M. emiliae clade; actually both taxa belong to separate lineages of Mico.

Our path sampling analysis clearly supports M. argentatus, M. emiliae, and M. leucippe as three separate species, considering that a Bayes factor > 10 is decisive44. Our results reject the hypothesis of only one species––M. emiliae-M. leucippeM. argentatus (BF = 367.46)––and the hypotheses of two species––M. argentatus and M. emiliae-M. leucippe (BF = 145.08), M. emiliae and M. leucippe-M. argentatus (BF = 99.44), or M. leucippe and M. argentatus-M. emiliae (BF = 348.29). These results support the unambiguous diagnosis of these three species according to our morphological data.

Distribution

The ranges of M. emiliae and Juruena–Teles Pires marmosets are separated by the Teles Pires River and in the headwaters of the Teles Pires River both are substituted by M. melanurus (Fig. 6; Supplementary Table S8). There is no evidence of range overlap between the Juruena–Teles Pires marmosets and any other Mico species. The distributions of M. emiliae and Juruena–Teles Pires marmosets are allopatric; M. emiliae is parapatric with M. leucippe around the Cachimbo highlands3 and both M. emiliae and the Juruena–Teles Pires marmosets are parapatric with M. melanurus at the extreme south of their distributions. Mico marcai46, M. rondoni21 and M. argentatus25 are allopatric to M. emiliae and the Juruena–Teles Pires marmosets, being separated by rivers and by the ranges of other Mico species.

Integrative approach in taxonomic hypothesis-testing and decision-making

The marmosets from the Juruena–Teles Pires interfluve have unique states of pelage colour characters when compared to all nominal species of Mico species, thus are clearly diagnosable, form a fully supported clade in our phylogenomic trees and are found only in the Juruena–Teles Pires interfluve, without evidence of range overlap with any other congeneric species. The criteria adopted here reject the null hypothesis that marmosets from the Juruena–Teles Pires interfluve are M. emiliae or another known species of Mico. We therefore describe them as a new species.

Order Primates Linnaeus, 1758

Family Callitrichidae Gray, 1821

Genus Mico Lesson, 1840

Mico schneideri sp. n. Costa-Araújo, Silva-Jr., Boubli, Rossi, Hrbek & Farias

urn:lsid:zoobank.org:act:9B4FFB49-FC65-45CC-862B-AA97E1C8F5BA

Holotype. INPA 7293, tissue CTGA 5934, field number RCA 60, adult female, stuffed skin, skull, skeleton. This specimen was collected on April 2nd, 2016 in an urban forest fragment located in Paranaíta city (09°41′21″ S, 56°29′10″ W), on the left margin of Teles Pires River, Mato Grosso State, Brazil, by Rodrigo Costa Araújo.

Type locality. Paranaíta municipality, left margin of the Teles Pires River, northern Mato Grosso State, Brazil (09°41′21”S, 56°29′10”W).

Figure 2

Schneider’s marmosets Mico schneideri sp. n. recorded at the type locality: Paranaíta, left margin of the Teles Pires River, Mato Grosso State, Brazil. (a) Adult female; (b) adult male. Photos: Diego Silva.

Table 1 Pelage colour characters from chromogenetic fields and their states in Mico schneideri sp. n. and in the morphologically and phylogenetically close related species.
Figure 3
figure3

Dorsal view of skins of Mico species tested for diagnosability of morphological characters of pelage colour. Left to right: Mico schneideri sp. n. holotype (INPA 7293), M. rondoni (MPEG 45620), M. marcai (MPEG 42807), M. emiliae (MPEG 45566), M. argentatus (MPEG 45609), and M. melanurus (MPEG 45571).

Figure 4
figure4

Bayesian phylogeny of the genus Mico inferred with ddRAD data, indicating the four main lineages of this genus in distinct colours (black lines are outgroups). Clades supported are indicated by black circles and unresolved branches (≤ 0.95 posterior probability) by white circles. Illustrations: Stephen Nash.

Figure 5
figure5

Two of the four lineages retrieved in genus Mico, based on morphological synapomorphies (data not shown) and phylogenomic analyses. (a) Mico emiliae lineage; (b) Mico schneideri sp. n. lineage. Illustrations: Stephen Nash.

Figure 6
figure6

Geographic distribution of Mico schneideri sp. n. and M. emiliae (see Supplementary Table S8 for locality details). Illustrations: Stephen Nash.

Paratypes. Urban forest fragment, Paranaíta city, left margin of Teles Pires River (09°41′21″ S, 56°29′10″ W): INPA 7294, tissue CTGA 5935, field number RCA 61, adult female; INPA 7295, tissue CTGA 5936, field number RCA 62, adult male; both preserved in fluid and collected on April 2nd, 2016 by Rodrigo Costa Araújo. Urban forest fragment, Alta Floresta city, left margin of Teles Pires River (09°51′50′′ S, 56º04′20′′ W): MPEG 24595, field number RA 41, subadult male, stuffed skin, skull; MPEG 24596, field number RA 42, subadult male, stuffed skin, skull; both collected on October 16, 1995 by R. Alperin, R. Rodrigues, and N. Silva. Urban forest fragment, Alta Floresta city, left margin of Teles Pires River (09°53′04′′ S, 56°04′21′′ W): UFMT 3851, field number RVR 40, adult male, stuffed skin, skeleton, and tissue, collected on May 6, 2014 by Rogério Rossi. Peri-urban forest fragment, Alta Floresta, left margin of Teles Pires River (09°58′57′′ S, 56°04′21′′ W): UFMT 4833, field number RVR 43, adult male, stuffed skin, skeleton, and tissue; UFMT 3852, field number RVR 44, adult male, stuffed skin, skeleton, and tissue; UFMT 4834, field number RVR 45, adult male, stuffed skin, skeleton, and tissue, collected on May 6, 2014 by Rogério Rossi. Ourolândia, left margin of Teles Pires River (10°23′26″ S, 56°24′28′′ W): MPEG 24606, field number RA 63, male, stuffed skin, collected on October 22 1995; MPEG 24608, field number RA 68, adult male, stuffed skin, skull; MPEG 24609, field number RA 69, adult female, stuffed skin, skull; MPEG 24610, field number RA 70, adult female, stuffed skin, skull; MPEG 24611, field number RA 71, adult male, stuffed skin, skull; all collected on October 23 1995 by R. Alperin, R. Rodrigues, and N. Silva.

Diagnosis. Uniform lead colour on saddle and rump, and underparts cream-silvery with orange hues.

Etymology. The new species is named in honour of Professor Horacio Schneider, a pioneer, and a major contributor to the phylogenetic studies of Neotropical Primates, who humbly accepted to have this species named in his honour.

Description of the holotype. Hairs on the face are short, mostly white but also black or bi-banded black-white, distributed all over the face, denser in circumbucal area, rhinarium and sides of the face, increasing in size towards the sides of the face; eumelanic vibrissae on the rhinarium, supraorbital region and along the zygomatic bone. Face tegument eumelanic in the centre of the supraorbital area, around the eyes, along the sides and the middle of the nose thrill, on the rhinarium and circumbucal area; dark brown eyes. White and long hairs on outer and inner pinnae, longer and denser on the inner surface, partially covering the pinnae; ear tufts absent; eumelanic tegument on a large proportion of each ear, but paler than the eumelanic tegument of the face. White hairs surrounding the face and on the sides of the head, longer than on the face; white hair on the head, covering the lower portion of the pinnae; black crown, separated from facial hairs by a horizontal line of white hairs. Gray mantle. Dorsal forearms greyish cream, blackish golden hairs on hands; ventral forelimb hairs cream, white on ventral neck and chest. Cream hairs on the belly. Saddle and rump of a uniform lead colour. Hairs on underparts cream-silvery on the anterior region, grading to light orange towards the posterior area on the dorsal and ventral hind limbs; ventral hind limb hairs pure orange on the posterior area, whereas pure cream on the anterior area. Goldenish orange hairs on feet. Blacktail with orange hairs on the ventral surface of tail insertion, an inch in length. The tegument is slightly eumelanic on the ventral surface of hands, unpigmented on the ventral surface of feet; claw-like nails, curved dorsoventrally in all digits except the hallux, which bears a flat nail.

Intra-specific morphological variation. There is only minor individual variation among the marmosets from the Juruena–Teles Pires interfluve manifested as the conspicuousness of the orangish tone over the basic cream colour of hairs in the chest, belly, and ventral underparts. In prepared skins, such variation is little perceptible, as well as the orangish colour of the underparts, whereas in fresh specimens the ventral region of fore and hind limbs and belly hairs can show a bright and vivid orange-cream colour. A small amount of cream hair can be observed on and around the ears, chest, and in an even smaller quantity on the mantle in the paratypes INPA 7294 and INPA 7295. There is also a tonal variation in the colour of the hairs on hands, feet, and lower portion of underparts of the paratypes deposited at MPEG, attributable to fading in storage, varying from goldenish orange to light orange on feet and posterior area of underparts, and varying from golden to light yellow on hands (see Fig. 2, Supplementary Fig. S9).

Geographic distribution. Mico schneideri sp. n. is endemic to the Juruena–Teles Pires interfluve, southern Amazonia, Mato Grosso State, Brazil. The species distribution is limited by the Juruena River to the west and by the Teles Pires River to the east, proceeding north to their confluence. The southern portion of the species range is less well-defined, but it extends to the headwaters of the Juruena and Teles Pires rivers, but no further south than the city of Lucas do Rio Verde. In this region, the Amazonia biome transitions to the Cerrado biome, and thus parapatry is expected between M. schneideri sp. n. and M. melanurus, the only species of Mico known to occur in the Cerrado.

Habitat. Primary and secondary terra firme forests, and Amazonia-Cerrado transitional forests.

Suggested vernacular names. Schneider’s marmoset (English); sagui-de-Schneider (Portuguese).

Mico emiliae is morphologically diagnosable, monophyletic, and allopatric along most of its range. Mico argentatus and M. leucippe are morphologically diagnosable and, although they were not retrieved as monophyletic in our phylogenetic inferences, path sampling analysis of genomic data associated with morphology and distribution data provide decisive support for their recognition as distinct species. Mico argentatus is allopatric on the east bank of the Xingu River and on the west bank of the Xingu River, this species is parapatric to M. leucippe––which is, in turn, apparently restricted to a narrow area between the Jamanxim and the Irirí-Curuá Rivers3,25. The distribution of M. leucippe is not limited by any conspicuous geographical barrier that could prevent introgression with M. argentatus or M. emiliae.

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