Does the widely distributed rodent <i><i>Calomys tener</i></i> (Cricetidae: Sigmodontinae) constitute a single evolutionary unit?

González-Ittig, Raul E.; Kandel, Narayan P.; Bonvicino, Cibele R.; Salazar-Bravo, Jorge

doi:10.3897/zoologia.36.e30354

Raul E. González-Ittig ^**Corresponding autor: Raúl E. González-Ittig (raulgonzalezittig@yahoo.com.ar)

Instituto de Diversidad y Ecología Animal, CONICET, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba. Avenida Vélez Sársfield 299, 5000JJC Córdoba, Argentina.

https://orcid.org/0000-0001-6761-3379

Narayan P. Kandel

Department of Biological Sciences, Texas Tech University. PO Box 43131, 79409 Lubbock, Texas, USA.

https://orcid.org/0000-0003-4373-1113

Cibele R. Bonvicino

Divisão de Genética, Instituto Nacional de Câncer. Rua André Cavalcanti 37, 4º andar, 20231-050 Rio de Janeiro, RJ, Brazil.

https://orcid.org/0000-0002-1948-7643

Jorge Salazar-Bravo

Department of Biological Sciences, Texas Tech University. PO Box 43131, 79409 Lubbock, Texas, USA.

https://orcid.org/0000-0001-5905-2532

^*Corresponding autor: Raúl E. González-Ittig (raulgonzalezittig@yahoo.com.ar)

Author Contributions:

REGI analyzed the data, wrote and revised the paper; NPK processed and analyzed the raw data in laboratory; CRB participated in original fieldwork and revised the paper; JSB conceived and designed the study and revised the paper.

Competing Interests:

The authors have declared that no competing interests exist.

Editorial responsibility:

Diego Astúa de Moraes

Figures (4)
Tables (1)

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Figure 1
Geographical locations of individuals listed in . Vegetation formations are represented by ecoregions like Cerrado, Humid Chaco, Rainforests (including the phytogeographic regions Alto Paraná Atlantic forest + Araucaria moist forest + Serra do Mar coastal forest), Dry Forests (Mato Grosso seasonal forest + Atlantic dry forest) and Savannas (Southern cone Mesopotamian savanna + Uruguayan savanna). The star indicates the type locality of Calomys tener: Lagoa Santa in the state of Minas Gerais corresponding to the Cerrado ecoregion. This map was designed using free spatial data of QGIS (Quantum GIS Development Team, 2018), available at: http://qgis.osgeo.org.

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Figure 2
Phylogram of the Bayesian consensus tree obtained from Cyt-b data set for species of Calomys with emphasis in Calomys tener. The order of the support values in the nodes is as follows: Bayesian posterior probabilities/maximum likelihood bootstrap/maximum parsimony bootstrap. Sequences from GenBank are indicated with their accession number and the species names. In the clade corresponding to C. tener the haplotype number, the specimen having each haplotype and the sampling locality is indicated. The vertical bars represent associations also observed in the network of , although with no statistical support. The intraspecific relationships recovered with the different phylogenetic methods are indicated.

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Figure 3
Median-joining network showing the relationships and relative abundance of the 28 haplotypes (indicated by a number) detected in Calomys tener. The different colors indicate the country where each haplotype was detected. Each bar through the solid line represents one nucleotide difference between haplotypes. The black circle (mv1) represents a median vector.

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Figure 4
Phylogram of the Bayesian consensus tree obtained from COI data set for species of Calomys with emphasis in Calomys tener. The order of the support values in the nodes is as follows: Bayesian posterior probabilities/maximum likelihood bootstrap/maximum parsimony bootstrap. Sequences from GenBank are indicated with their accession number and the species names. In the clade corresponding to C. tener the haplotype letter, the specimen having each haplotype and the sampling locality is indicated.

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Table 1
Field identification code or voucher numbers of specimens of the Delicate Vesper Mouse (Calomys tener). The location of the sampling sites shown in with provinces or departments in parentheses; geographic coordinates; Cyt-b GenBank accession numbers (there are five accession numbers corresponding to the cytochrome oxidase I gene indicated in parenthesis with COI) and articles were the sequences were obtained.

Specimen ID	Sample Location	Latitude	Longitude	GenBank registers	Haplotype	Reference
	Brazil
CRB1549	1- Jaborandi (Bahia)	-13.6188	-44.4328	DQ447298	20	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
CRB1558	1- Jaborandi (Bahia)	-13.6188	-44.4328	DQ447299	21	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
CRB1584	1- Jaborandi (Bahia)	-13.6188	-44.4328	DQ447300	22	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
CRB1590	1- Jaborandi (Bahia)	-13.6188	-44.4328	DQ447301	23	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
AN2557	2- Aliança do Tocantins (Tocantins)	-11.0050	-48.9333	AY964055	12	Haag et al. (2007Haag T, Muschner VC, Freitas LB, Oliveira LFO, Langguth AR, Mattevi M (2007) Phylogenetic relationships among species of the genus Calomys with emphasis on South American lowland taxa. Journal of Mammalogy 88(3): 769-776. https://doi.org/10.1644/05-MAMM-A-319R1.1 https://doi.org/10.1644/05-MAMM-A-319R1.... )
MN36437	3- Serra da Mesa (Goiás)	-13.8341	-48.3044	AY964053	10	Haag et al. (2007Haag T, Muschner VC, Freitas LB, Oliveira LFO, Langguth AR, Mattevi M (2007) Phylogenetic relationships among species of the genus Calomys with emphasis on South American lowland taxa. Journal of Mammalogy 88(3): 769-776. https://doi.org/10.1644/05-MAMM-A-319R1.1 https://doi.org/10.1644/05-MAMM-A-319R1.... )
CRB2382	4- Mimoso de Goiás (Goiás)	-15.0483	-48.0833	DQ447302	24	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
MNRJ67075/CRB2382	4- Mimoso de Goiás (Goiás)	-15.0483	-48.0833	GU938935 (COI)	A	Muller et al. (2013Müller L, Gonçalves GL, Cordeiro-Estrela P, Marinho JR, Althoff SL, Testoni AF, González EM, Freitas TRO (2013) DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS ONE 8(11): e80282. https://doi.org/10.1371/journal.pone.0080282 https://doi.org/10.1371/journal.pone.008... )
CRB503	5- Corumbá de Goiás (Goiás)	-15.9241	-48.8085	DQ447295	17	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
CRB495	5- Corumbá de Goiás (Goiás)	-15.9241	-48.8085	KX987844	18	This study
FMRP-USP96	6- Franca (São Paulo)	-20.5333	-47.4000	KX987845	15	This study
CPV425	7- Cajuru (São Paulo)	-21.2540	-47.3104	KX987842	13	This study
CPV432	7- Cajuru (São Paulo)	-21.2540	-47.3104	KX987843	14	This study
CRB1219	8- Pedreira (São Paulo)	-22.7419	-46.9014	DQ447296	13	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
CRB1220	8- Pedreira (São Paulo)	-22.7419	-46.9014	DQ447297	19	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
EM1135	9- Campinas (São Paulo)	-22.9008	-47.0572	DQ447294	16	Almeida et al. (2007Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and Temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of open/dry biomes of South America. Molecular Phylogenetics and Evolution 42(2): 449-466. https://doi.org/10.1016/j.ympev.2006.07.005 https://doi.org/10.1016/j.ympev.2006.07.... )
LDCM-AB6	10- Capão Bonito (São Paulo)	-24.0600	-48.3200	GU939000 (COI)	C	Muller et al. (2013Müller L, Gonçalves GL, Cordeiro-Estrela P, Marinho JR, Althoff SL, Testoni AF, González EM, Freitas TRO (2013) DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS ONE 8(11): e80282. https://doi.org/10.1371/journal.pone.0080282 https://doi.org/10.1371/journal.pone.008... )
LDCM-AB519	10- Capão Bonito (São Paulo)	-24.0600	-48.3200	GU939001 (COI)	C	Muller et al. (2013Müller L, Gonçalves GL, Cordeiro-Estrela P, Marinho JR, Althoff SL, Testoni AF, González EM, Freitas TRO (2013) DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS ONE 8(11): e80282. https://doi.org/10.1371/journal.pone.0080282 https://doi.org/10.1371/journal.pone.008... )
LDCM-AB10	10- Capão Bonito (São Paulo)	-24.0600	-48.3200	GU939002 (COI)	B	Muller et al. (2013Müller L, Gonçalves GL, Cordeiro-Estrela P, Marinho JR, Althoff SL, Testoni AF, González EM, Freitas TRO (2013) DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS ONE 8(11): e80282. https://doi.org/10.1371/journal.pone.0080282 https://doi.org/10.1371/journal.pone.008... )
NK42183	11- Tupi Paulista (São Paulo)	-21.3873	-51.5678	AF385597	9	Salazar-Bravo et al. (2001Salazar-Bravo J, Dragoo JW, Tinnin DS, Yates TL (2001) Phylogeny and evolution of the Neotropical rodent genus Calomys: inferences from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 20(2): 173-184. https://doi.org/10.1006/mpev.2001.0965 https://doi.org/10.1006/mpev.2001.0965... )
NK42140	11- Tupi Paulista (São Paulo)	-21.3873	-51.5678	AF385596	8	Salazar-Bravo et al. (2001Salazar-Bravo J, Dragoo JW, Tinnin DS, Yates TL (2001) Phylogeny and evolution of the Neotropical rodent genus Calomys: inferences from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 20(2): 173-184. https://doi.org/10.1006/mpev.2001.0965 https://doi.org/10.1006/mpev.2001.0965... )
MCN-MAM42	12- Banhado Grande (Rio Grande do Sul)	-30.0117	-50.9650	JX975467	25	Quintela et al. 2014Quintela FM, da Silveira EC, Dellagnese DG, Cademartori CV (2014) Calomys tener (Winge, 1887) (Rodentia: Cricetidae:Sigmodontinae): Filling gaps. Check List 10(3): 650-654. https://doi.org/10.15560/10.3.650 https://doi.org/10.15560/10.3.650...
AFV02	13- Quintão (Rio Grande do Sul)	-29.6666	-50.2666	AY964054	11	Haag et al. (2007Haag T, Muschner VC, Freitas LB, Oliveira LFO, Langguth AR, Mattevi M (2007) Phylogenetic relationships among species of the genus Calomys with emphasis on South American lowland taxa. Journal of Mammalogy 88(3): 769-776. https://doi.org/10.1644/05-MAMM-A-319R1.1 https://doi.org/10.1644/05-MAMM-A-319R1.... )
UFPB7407/JR405	14- Alegrete (Rio Grande do Sul)	-29.5700	-55.7100	GU938944 (COI)	D	Muller et al. (2013Müller L, Gonçalves GL, Cordeiro-Estrela P, Marinho JR, Althoff SL, Testoni AF, González EM, Freitas TRO (2013) DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS ONE 8(11): e80282. https://doi.org/10.1371/journal.pone.0080282 https://doi.org/10.1371/journal.pone.008... )
	Argentina
34769	15- Leandro N Alem (Misiones)	-27.5833	-55.2667	KF917370	6	González-Ittig et al. (2014González-Ittig RE, Kandel N, Levis S, Calderon G, Salazar-Bravo J, Gardenal CN (2014). Molecular systematic of the South American rodent Calomys laucha (Cricetidae: Sigmodontinae), a reservoir of the Laguna Negra hantavirus. Canadian Journal of Zoology 92(12): 1093-1098. https://doi.org/10.1139/cjz-2014-0133 https://doi.org/10.1139/cjz-2014-0133... )
LTU687	16- Estancia Santa Inés (Misiones)	-27.5256	-55.8719	KX987847	2	This study
LTU692	16- Estancia Santa Inés (Misiones)	-27.5256	-55.8719	KX987848	3	This study
LTU711	16- Estancia Santa Inés (Misiones)	-27.5256	-55.8719	KX987849	4	This study
LTU726	16- Estancia Santa Inés (Misiones)	-27.5256	-55.8719	KX987850	5	This study
LTU341	17- RN 12 y Arroyo Itaembé Miní (Misiones)	-27.4300	-56.0000	KX987856	1	This study
LTU342	17- RN 12 y Arroyo Itaembé Miní (Misiones)	-27.4300	-56.0000	KX987846	1	This study
	Paraguay
TK66069	18- Estancia San Felipe, 2km S house (Ñeembucú)	-27.1833	-58.3833	KF917377	28	González-Ittig et al. (2014González-Ittig RE, Kandel N, Levis S, Calderon G, Salazar-Bravo J, Gardenal CN (2014). Molecular systematic of the South American rodent Calomys laucha (Cricetidae: Sigmodontinae), a reservoir of the Laguna Negra hantavirus. Canadian Journal of Zoology 92(12): 1093-1098. https://doi.org/10.1139/cjz-2014-0133 https://doi.org/10.1139/cjz-2014-0133... )
TK63733	19- Reserva Natural Privada Ypeti (Caazapá)	-25.6825	-55.5300	KX987852	26	This study
TK63769	20- Estancia Golondrina (Caazapá)	-25.6010	-55.4865	KX987853	27	This study
TK63984	21- Res. Nat. del Bosque Mbaracayu (Canindeyú)	-24.1601	-55.2832	KF917376	12	González-Ittig et al. (2014González-Ittig RE, Kandel N, Levis S, Calderon G, Salazar-Bravo J, Gardenal CN (2014). Molecular systematic of the South American rodent Calomys laucha (Cricetidae: Sigmodontinae), a reservoir of the Laguna Negra hantavirus. Canadian Journal of Zoology 92(12): 1093-1098. https://doi.org/10.1139/cjz-2014-0133 https://doi.org/10.1139/cjz-2014-0133... )
	Bolivia
NK21054	22- Santa Rosa de La Roca (Santa Cruz)	-16.0500	-61.5667	AF385595	7	Salazar-Bravo et al. (2001Salazar-Bravo J, Dragoo JW, Tinnin DS, Yates TL (2001) Phylogeny and evolution of the Neotropical rodent genus Calomys: inferences from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 20(2): 173-184. https://doi.org/10.1006/mpev.2001.0965 https://doi.org/10.1006/mpev.2001.0965... )

[1] ^*Corresponding autor: Raúl E. González-Ittig (raulgonzalezittig@yahoo.com.ar)

Brasil

Brasil

Does the widely distributed rodent Calomys tener (Cricetidae: Sigmodontinae) constitute a single evolutionary unit?

ABSTRACT