Abstract
The genus Gracilinanus ranges from savannas to dense forests in South America, yet its systematics have never been thoroughly investigated across its wide distributional range. We assessed Gracilinanus phylogenetic relationships, species boundaries, and geographical limits using mtDNA sequences. Our analysis confirmed the distinctiveness of the six recognized species (G. aceramarcae, G. agilis, G. emiliae, G. marica, G. microtarsus, and G. peruanus), with a mean p-distance for interspecific nucleotide sequence divergences ranging from 13–16.2% and robust phylogenetic support (BPP > 0.95; BS > 75%). Refined species delimitation approaches (GMYC, PTP, ASAP) revealed potential cryptic diversity, suggesting up to 20 candidate species. Three geographically structured and divergent lineages (4.1–4.8% sequence divergence) were identified within G. agilis, extending its Cerrado range. Within G. emiliae, we found divergence values ranging from 4.7–5.7% and the first known record for the northeastern Atlantic Forest. Three divergent clades were recovered within G. microtarsus (9.0–9.8% sequence divergence), including a new lineage for the northern Atlantic Forest. For G. peruanus, we found two divergent lineages (7.2%) and the first documented occurrence for Amazonian lowland forest. This comprehensive sampling revealed greater genetic diversity in Gracilinanus, extending its geographic limits. Here we propose nine putative new species, emphasizing a hidden diversity that warrants formal description and further increases the taxonomic diversity of this genus. These newly identified lineages underscore the urgency of inventorying and conserving the threatened ecosystems of the Cerrado and Atlantic Forest hotspots.
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Data availability
Sequence data are deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and are publicly available. Datasets generated and/or analyzed during the current study are also available from the corresponding author upon request.
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Acknowledgements
We would like to thank the researchers and curators of the mammalogical scientific collections for tissue samples and accession to vouchers, namely: Juliana Gualda and Dr. Mario de Vivo (MZUSP), Dr. Miguel T. Rodrigues (IBUSP), Dr. Alexandre R. Percequillo (LAMA), Dr. Ana Cristina Mendes-Oliveira (UFPA), and Dr. Cláudia Silva (IEPA). We also would like to thank all researchers and students who contributed in the field, surveying Gracilinanus specimens; to Renato K. Kimura and Silas C. Príncipe for technical support in the laboratory at UFSCar. To George M.T. Mattox and Mercival R. Francisco for their contributions as committee members of the LEF graduation thesis. To Monique R. Brito and Milena C. Telhe for the support in the analyses of the molecular species delimitation approaches.
Funding
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, #88887.615416/2021-00, Conselho Nacional de Desenvolvimento Científico e Tecnológico,grants #107282/2017-8, #408648/2023-6, #457444/2012-6; Fundação de Amparo à Pesquisa do Estado de São Paulo, #98/05075-7; #00/06642-4; #2011/20022-3; #2015/21259-8; #2017/23548-2; #2018/14091-1; #2020/12658-4; #2020/01378-0; #2022/12632-0.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study’s conception and design. Tissue acquisition was performed by Ana Paula Carmignotto. Material preparation, data collection, and edition of figures were performed by all authors. Analyses were performed by Larissa Eler Fernandes and writing was performed by all authors. All authors commented on previous versions of the manuscript, reading and approving the final manuscript.
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The authors declare no competing interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10914_2024_9706_MOESM1_ESM.xlsx
Online Resource 1: Pairwise K2P divergence values (%) - mean (and range) - among lineages for G. agilis, G. emiliae, G. microtarsus and G. peruanus. (XLSX 17.3 KB)
10914_2024_9706_MOESM3_ESM.docx
Online Resource 3: Geographically-structured clades for G. microtarsus across altitudinal and mountain ranges. (DOCX 11.3 KB)
10914_2024_9706_MOESM4_ESM.docx
Online Resource 4: Time-scaled, fossil-calibrated phylogeny of Gracilinanus. Mean divergence (Ma, above nodes) and range (95% HPD, below nodes). (DOCX 12.2 KB)
Appendix 1
Appendix 1
List of localities of Gracilinanus specimens with DNA sequence data analyzed in the present study.
Number as in the map of Fig. 1. Information is presented in the following format: state or province, department or municipality, locality [geographic coordinates, with underline indicating coordinates not referred to the specific locality]: mtDNA lineage – field or voucher number.
Brazil
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1.
Alagoas, Passo de Camaragibe, Barra de Camaragibe [09° 19’ S, 35° 25’ W]: Gracilinanus emiliae – PCM 05.
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2.
Amapá, Ferreira Gomes, Igarapé do Braço, Floresta Nacional do Amapá [01º 18’ S, 51º 35’ W]: Gracilinanus emiliae – KC 96.
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3.
Bahia, Camacan, Reserva Serra Bonita [15° 24’ S, 39° 29’ W]: Gracilinanus microtarsus – MTR 15893.
-
4.
Bahia, Caetité, Caetité [14° 04’ S, 42° 29’ W): Gracilinanus agilis – LBCE 3817.
-
5.
Bahia, Andaraí, Fazenda Santa Rita, 8 km E Andaraí [12° 48’ S, 41° 16’ W]: Gracilinanus agilis – UFMG 2496.
-
6.
Bahia, Jaborandi, Fazenda Sertão do Formoso [14° 48’ S, 45º 57’ W]: Gracilinanus agilis – CRB 1571.
-
7.
Bahia, Morro do Chapéu, Morro do Chapéu [11° 36’ S, 41° 12’ W]: Gracilinanus microtarsus – MTR 22561.
-
8.
Bahia, Rio de Contas, Rio de Contas [13° 35’ S, 41° 48’ W]: Gracilinanus agilis – MN 67593 (JAO 1171).
-
9.
Bahia, Jussari, RPPN Serra do Teimoso [15° 09’ S, 39° 31’ W]: Gracilinanus microtarsus – ST 207.
-
10.
Ceará, Crato, Chapada do Araripe 7 km SW Crato [07° 17’ S, 39° 27’ W]: Gracilinanus agilis – UFMG 2504.
-
11.
Ceará, Jaguaruana, Jaguaruana [04° 50’ S, 37° 47’ W]: Gracilinanus agilis – LBCE 5254.
-
12.
Espírito Santo, Castelo, Parque Estadual do Forno Grande [20° 30’ S, 41° 06’ W]: Gracilinanus microtarsus – LPC 1447.
-
13.
Espírito Santo, Serra, Área de Proteção Ambiental do Mestre Álvaro [20° 10’ S, 40° 19’ W]: Gracilinanus microtarsus – LPC 1410.
-
14.
Espírito Santo, Águia Branca, Mata da Lagoa, Sítio Krok [18° 58’ S, 40° 44’ W]: Gracilinanus microtarsus – YL 419.
-
15.
Espírito Santo, Ibiraçu, Morro da Vargem, Mosteiro Zen Budista [19° 50’ S, 40° 22’ W]: Gracilinanus microtarsus – MBML 2716.
-
16.
Espírito Santo, Domingos Martins, Parque Estadual de Pedra Azul [20° 24’ S, 40° 58’ W]: Gracilinanus microtarsus – UFES-CTA 831.
-
17.
Espírito Santo, Cariacica, Reserva Biológica Duas Bocas [20° 17’ S, 40° 31’ W]: Gracilinanus microtarsus – LPC 1092.
-
18.
Espírito Santo, Sooretama, Reserva Natural da Vale [19° 12’ S, 40° 06’ W]: Gracilinanus microtarsus – TAX 15.
-
19.
Espírito Santo, São José do Calçado, Sapucaia, Alegoria [21° 02’ S, 41° 43’ W]: Gracilinanus microtarsus – LPC 1377.
-
20.
Goiás, Cachoeira Alta, Cachoeira Alta [18° 43’ S, 51° 19’ W]: Gracilinanus agilis – CM 598.
-
21.
Goiás, Anápolis, Anápolis [16° 19’ S, 48° 58’ W]: Gracilinanus agilis – LBCE 9469.
-
22.
Goiás, Aporé, Aporé [18° 57’ S, 51° 55’ W]: Gracinanus agilis – LBCE 11947.
-
23.
Goiás, Cavalcante, Fazenda Fiandeira, Parque Nacional da Chapada dos Veadeiros, 65 km SSW Cavalcante [14° 04’ S, 47° 45’ W]: Gracilinanus agilis – CRB 895.
-
24.
Goiás, Luziânia, Luziânia [16° 14’ S, 47° 55’ W]: Gracilinanus agilis – LBCE 7500.
-
25.
Goiás, São Domingos, São Domingos [13° 23’ S, 46° 19’ W]: Gracilinanus agilis – LBCE 11997.
-
26.
Goiás, Caldas Novas, Usina Hidrelétrica de Corumbá 30 km SE Caldas Novas [17° 59’ S, 48° 31’ W]: Gracilinanus agilis – UHECO 4722.
-
27.
Goiás, Minaçu, Usina Hidrelétrica de Serra da Mesa [13° 49’ S, 48° 18’ W]: Gracilinanus agilis – UHESM 1759.
-
28.
Maranhão, Açailândia, Açailândia [04° 57’ S, 47° 30’ W]: Gracilinanus agilis – UFPAM 507.
-
29.
Maranhão, Carolina, Parque Nacional Chapada das Mesas [07° 19’ S, 47° 20’ W]: Gracilinanus agilis – APC 2340.
-
30.
Mato Grosso, Jaciara/Juscimeira, Jaciara/Juscimeira [16° 07’ S, 55° 01’ W]: Gracilinanus agilis – UFMT 3817.
-
31.
Mato Grosso, Poconé, Parque Nacional do Pantanal [17° 51’ S, 57° 25’ W]: Gracilinanus agilis – MZUSP 35192.
-
32.
Mato Grosso, Aripuanã, Serra do Expedito, 25 km Aripuanã [11° 03’ S, 59° 30’ W]: Gracilinanus peruanus – UFMT 1379.
-
33.
Mato Grosso, Poconé, Base de Pesquisas do Pantanal CENAP/IBAMA 110 km SSW Poconé [18° 45’ S, 57° 22’ W]: Gracilinanus agilis – UFMG 2497.
-
34.
Mato Grosso, Alto Araguaia, Fazenda Água Limpa [15° 17’ S, 58° 37’ W]: Gracilinanus peruanus – INPA 6740.
-
35.
Mato Grosso, Jauru, Fazenda Alto Jauru [15° 27’ S, 58° 26’ W]: Gracilinanus peruanus – INPA 6736.
-
36.
Mato Grosso, Araputanga, Fazenda Araputanga [15° 21’ S, 58° 26’ W]: Gracilinanus peruanus – INPA 6739.
-
37.
Mato Grosso, Barra do Garças, Fazenda Eldorado [15° 35’ S, 52° 17’ W]: Gracilinanus agilis – UFMT 2043.
-
38.
Mato Grosso, Araputanga, Fazenda Quatro Meninas [15° 20’ S, 58° 33’ W]: Gracilinanus peruanus – INPA 6741.
-
39.
Mato Grosso, Primavera do Leste, Margem esquerda do Rio Cumbuco [15° 13’ S, 54° 03’ W]: Gracilinanus agilis – UFMT 1039.
-
40.
Mato Grosso do Sul, Aquidauana, Aquidauana [20° 28’ S, 55º 47’ W]: Gracilinanus agilis – LBCE 4888.
-
41.
Mato Grosso do Sul, Cassilândia, Cassilândia [19° 06’ S, 51° 44’ W]: Gracilinanus agilis – LBCE 11949.
-
42.
Mato Grosso do Sul, Corumbá, Corumbá [19° 01’ S, 57° 39’ W]: Gracilinanus agilis – LBCE 5665.
-
43.
Mato Grosso do Sul, Rio Miranda, acima Passo do Lontra [19° 34’ S, 57° 00’ W]: Gracilinanus agilis – UFMG 2500.
-
44.
Minas Gerais, Itamonte, Itamonte [22° 17’ S, 44° 52’ W] Gracilinanus microtarsus – MP 499.
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45.
Minas Gerais, Aiuruoca, Aiuruoca [21° 58’ S, 44° 36’ W] Gracilinanus microtarsus – MP 329.
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46.
Minas Gerais, Brasilândia de Minas, Brasilândia de Minas [17° 01’ S, 46° 01’ W]: Gracilinanus agilis – MCNM 2189.
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47.
Minas Gerais, Bocaiúva, Fazenda Corredor, Distrito Carne Seca [17° 06’ S, 43° 49’ W]: Gracilinanus agilis – UFMG 2433.
-
48.
Minas Gerais, Lagoa Santa, Fazenda das Bicas [19° 38’ S, 43° 53’ W]: Gracilinanus microtarsus – EDH 12.
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49.
Minas Gerais, João Pinheiro, João Pinheiro [17° 44’ S, 46° 10’ W]: Gracilinanus agilis – MCNM 2243.
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50.
Minas Gerais, Nova Ponte, Mata do Vasco, 12 km W Nova Ponte [19° 08’ S, 47° 40’ W]: Gracilinanus agilis – MVZ 197439.
-
51.
Minas Gerais, Belo Horizonte, Parque Aggeo Pio Sobrinho [19° 59’ S, 43° 58’ W]: Gracilinanus microtarsus – LPC 915.
-
52.
Minas Gerais, Santa Barbara, Parque do Caraça [19° 58’ S, 43° 25’ W]: Gracilinanus microtarsus – NM 04.
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53.
Minas Gerais, São Gonçalo do Rio Preto, Parque Estadual do Rio Preto, 15 km S São Gonçalo do Rio Preto [18º 09’ S, 43° 23’ W]: Gracilinanus agilis – UFMG 2493.
-
54.
Minas Gerais, Coronel Murta, Ponte do Colatino, margem esquerda do Rio Jequitinhonha [16° 36’ S, 42° 12’ W]: Gracilinanus agilis – UFMG 2495.
-
55.
Minas Gerais, Tiradentes, Tiradentes [21º 07’ S, 44° 10’ W]: Gracilinanus microtarsus – MP 538.
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56.
Minas Gerais, Lavras, Universidade Federal de Lavras [21° 14’ S, 44º 59’ W]: Gracilinanus microtarsus – MP 79.
-
57.
Pará, Santana do Araguaia, Fazenda Santa Fé [9° 38’ S, 50° 08’ W]: Gracilinanus emiliae – FSF 92 m.
-
58.
Pará, São Félix do Xingu, Terra do Meio [05° 52’ S, 52° 47’ S]: Gracilinanus emiliae – RBM 1141.
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59.
Paraná, Ortigueira, Ortigueira [24° 13’ S, 50° 55’ W]: Gracilinanus microtarsus – ITM 192.
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60.
Paraná, Pinhalão, Pinhalão [23° 47’ S, 50° 02’ W]: Gracilinanus microtarsus – ITM 014.
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61.
Pernambuco, Buíque, Buíque, Parque Nacional do Catimbau [08° 35’ S, 37° 14’ W]: Gracilinanus agilis – AP 614.
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62.
Piauí, Bom Jesus, Estação Ecológica de Uruçuí-Una, [08° 51’ S, 44° 58’ W]: Gracilinanus agilis – MZUSP 30484.
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63.
Piauí, João Costa, João Costa [08° 03’ S, 42° 25’ W]: Gracilinanus agilis – LBCE 1240.
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64.
Piauí, Guaribas, Parque Nacional Serra das Confusões [09° 12’ S, 43° 29’ W]: Gracilinanus agilis – DAM 23 e ARP 73.
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65.
Rio de Janeiro, Rio de Janeiro, Pedra Branca-Colônia [22° 56’ S, 43° 29’ W]: Gracilinanus microtarsus – LBCE 4093.
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66.
Rio de Janeiro, Teresópolis, Teresópolis [22° 25’ S, 42° 58’ W]: Gracilinanus microtarsus – LBCE 6662.
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67.
Rondônia, Chupinguaia, Chupinguaia [12° 14’ S, 60° 44’ W]: Gracilinanus peruanus – UFMT 3816.
-
68.
Rondônia, Porto Velho, Estação Ecológica Mujica Nava [09° 26’ S, 64° 58’ W]: Gracilinanus peruanus – MJ 27.
-
69.
Rondônia, Porto Velho, Usina Hidrelétrica de Jirau [09° 20’ S, 64° 43’ W]: Gracilinanus peruanus – MJ 74.
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70.
São Paulo, Capão Bonito, Base do Carmo, Fazenda Intervales [24° 20’ S, 48° 25’ W]: Gracilinanus microtarsus – MVZ 182056.
-
71.
São Paulo, Águas de Santa Bárbara, Estação Ecológica de Santa Bárbara [22° 48’ S, 49° 14’ W]: Gracilinanus agilis – APC 2614 and Gracilinanus microtarsus – APC 2403.
-
72.
São Paulo, Sorocaba, Floresta Nacional de Ipanema [23° 26’ S, 47° 37’ W]: Gracilinanus microtarsus – APC 1753.
-
73.
São Paulo, Pinhalzinho, Pinhalzinho [22° 47’ S, 45° 35’ W]: Gracilinanus microtarsus – CIT 974.
-
74.
São Paulo, Cotia, Reserva Florestal do Morro Grande [23° 39’ S, 47° 01’ W]: Gracilinanus microtarsus – AB 343.
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75.
São Paulo, Santo André, Santo André [23° 40’ S, 46° 32’ W]: Gracilinanus microtarsus – StoAn 46.
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76.
São Paulo, Ribeirão Grande, Sitio Paulino [24° 06’ S, 48° 23’ W]: Gracilinanus microtarsus – FB 373.
-
77.
São Paulo, Sorocaba, Universidade Federal de São Carlos [23° 35’ S, 47° 31’ W]: Gracilinanus microtarsus – APC 2026.
-
78.
São Paulo, Matão, Matão [21° 36’ S, 48° 22’ W]: Gracilinanus microtarsus – PF 3850.
-
79.
Tocantins, Aliança do Tocantins, Aliança do Tocantins [11° 18’ S, 48º 56’ W]: Gracilinanus agilis – BR-153 132.
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80.
Tocantins, Lagoa da Confusão, Lagoa da Confusão [10° 47’ S, 49° 37’ W]: Gracilinanus agilis – RGR 426.
-
81.
Tocantins, Parque Nacional do Araguaia [10° 27’ S, 50° 29’ W]: Gracilinanus agilis – MN 60506 (ARB 48) and Gracilinanus agilis – MN 66268 (ARB 71).
-
82.
Tocantins, Pium, Parque Estadual do Cantão [9° 59’ S, 50° 02’ W]: Gracilinanus agilis – UFESMAM 1412.
Peru
83. Junín, Cordilheira de Vilcabamba [11° 40’ S, 73º 40’ W]: Gracilinanus aceramarcae – MUSM 13002.
84. Loreto, Nuevo San Juan, Rio Galvez [05° 15’ S, 73° 10’ W]: Gracilinanus emiliae – MUSM 15292.
Venezuela
85. Falcón, Serranía de San Luis, Parque Nacional J. C. ca. 10 km W + 4 km N Cabure, Sector Cerro Galicia [11° 11’ N, 69° 42’ W]: Gracilinanus marica – EBRG 24864.
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Fernandes, L.E., Lessinger, A.C. & Carmignotto, A.P. New data from South American hotspots uncover a greater diversity in Gracilinanus (Didelphimorphia: Didelphidae) mouse opossums. J Mammal Evol 31, 13 (2024). https://doi.org/10.1007/s10914-024-09706-7
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DOI: https://doi.org/10.1007/s10914-024-09706-7