Abstract
Genetic studies in the highlands of Mexico have revealed extensive intraspecific differentiation and highly structured genetic variation in rodents and other taxa. One of the most important and complex systems in these highlands is the Trans-Mexican Volcanic Belt (TMVB), a biogeographic region located in central Mexico. Recent studies suggest strong structure and undiscovered diversity within the TMVB highlands, which indicates more study of endemic species is warranted. One of these species is the endemic Volcano Harvest Mouse Reithrodontomys chrysopsis, which inhabits small and fragmented patches at high altitudes. This mouse is poorly known, under-represented in field collections, and has been the subject of few studies of phylogenetics, taxonomy, and evolutionary history. This study aimed to assess the phylogenetic and intraspecific relationships of R. chrysopsis throughout its known geographic distribution to better understand the evolutionary patterns of it and other TMVB mammals. Our phylogenetic analyses using Cytb and Fgb-I7 markers revealed that R. chrysopsis is sister to R. sumichrasti and R. megalotis, which contrasts with a previous hypothesis based on morphological data. Genetic differentiation, divergence time, and species delimitation analyses showed three main divergent lineages within R. chrysopsis, located at the western, central, and eastern TMVB. These lineages diverged during the Pliocene-Pleistocene interval. Our results support the hypothesis that volcanic activity and climatic oscillations during the Pleistocene in central Mexico promoted diversification processes within the TMVB. Further molecular and morphological studies will be needed to provide information for the taxonomic designation of the east divergent lineage detected herein.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and supplementary information file and are available from the corresponding author upon reasonable request. The sequences generated and analyzed during the current study are openly available in GenBank under accession numbers OP938697-OP938732. Additional data downloaded from GenBank and specimen information are available in Online Resource 1.
References
Álvarez-Castañeda ST, Álvarez T, González-Ruiz N (2015) Keys for Identifying Mexican Mammals. Centro de Investigaciones Biológicas del Noroeste and S. C. Asociación Mexicana de Mastozoología AC, Guadalajara, Jalisco.
Arellano E, González-Cozátl FX, Rogers DS (2005) Molecular systematics of Middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 37(2):529–540. https://doi.org/10.1016/j.ympev.2005.07.021
Arellano E, Almendra AL, Martínez-Borrego D, González-Cozátl FX, Rogers DS (2023). Revisiting species delimitation within Reithrodontomys sumichrasti (Rodentia: Cricetidae) using molecular and ecological evidence. Therya 14(1):161–179. https://doi.org/10.12933/therya-23-2236
Arriaga-Jiménez A, Rös M, Halffter G (2018) High variability of dung beetle diversity patterns at four mountains of the Trans-Mexican Volcanic Belt. PeerJ 6:e4468. https://doi.org/10.7717/peerj.4468
Arriola-Padilla V, Estrada-Martínez E, Ortega-Rubio A, Pérez-Miranda R, Gijón-Hernández AR (2014) Deterioro en áreas naturales protegidas del centro de México y del Eje Neovolcánico Transversal. Investig Cienc Univ Autón Aguascalientes 22(60):37–49
Baker RJ, Bradley RD (2006) Speciation in mammals and the genetic species concept. J Mammal 87(4):643–662. https://doi.org/10.1644/06-MAMM-F-038R2.1
Blair C, Bryson RW, Linkem CW, Lazcano D, Klicka J, McCormack JE (2019) Cryptic diversity in the Mexican highlands: thousands of UCE loci help illuminate phylogenetic relationships, species limits and divergence times of montane rattlesnakes (Viperidae: Crotalus). Mol Ecol Resour 19(2):349–365. https://doi.org/10.1111/1755-0998.12970
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina, A et al (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15(4):e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Bradley RD, Ordóñez-Garza N, Ceballos G, Rogers DS, Schmidly DJ (2017) A new species in the Peromyscus boylii species group (Cricetidae: Neotominae) from Michoacán, México. J Mammal 98(1):154–165. https://doi.org/10.1093/jmammal/gyw160
Castleberry SB, King TL, Wood PB, Ford WM (2002) Microsatellite DNA analysis of population structure in Allegheny woodrats (Neotoma magister). J Mammal 83(4):1058–1070. https://doi.org/10.1644/1545-1542(2002)083>1058:MDAOPS<2.0.CO;2
Challenger A, Caballero J (1998) Utilización y Conservación de los Ecosistemas Terrestres de México: Pasado, Presente y Futuro. Comisión Nacional para el Concimiento y Uso de la Biodiversidad, México, DF
Crameri S, 2018. Display the DISSECT/speciesDA.jar similarity matrix. GitHub Repository. https://github.com/scrameri/smtools/tree/master/SpeciesDelimitation. Accessed 23 September 2020
Espinosa D, Ocegueda S (2007) Introduction. In: Luna I, Morrone JJ, Espinosa D (eds) Biodiversidad de la Faja Volcánica Transmexicana. Universidad Nacional Autónoma de México, México, DF, pp 5–6
Fa JE, Morales J (1991) Mammals and Protected Areas in the Trans-Mexican Neovolcanic Belt. University of Oklahoma Press, Oklahoma
Fa JE, Morales J (1993). Patterns of mammalian diversity in Mexico. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological Diversity of Mexico: Origins and Distribution. Oxford University Press, New York, pp 319–361
Ferrusquía–Villafranca I (2007) Ensayo sobre la caracterización y significación biológica. In: Luna I, Morrone JJ, Espinosa D (eds) Biodiversidad de la Faja Volcánica Transmexicana. Universidad Nacional Autónoma de México, Mexico, DF, pp 7–24
Flores-Villela O (1993) Herpetofauna of Mexico: distribution and endemism. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds). Biological Diversity of Mexico: Origins and Distribution. Oxford University Press, New York, pp 253–280
Flores-Villela O, Gerez P (1994) Biodiversidad y Conservación en México: Vertebrados, Vegetación y Uso del Suelo. Comisión Nacional para el Conocimiento de la Biodiversidad, Mexico, DF
Gámez N, Escalante T, Rodríguez G, Linaje M, Morrone JJ (2012) Caracterización biogeográfica de la Faja Volcánica Transmexicana y análisis de los patrones de distribución de su mastofauna. Rev Mex Biodivers 83(1):258–272
García-Palomo A, Macías JL, Garduño VH (2000) Miocene to recent structural evolution of the Nevado de Toluca volcano region, central Mexico. Tectonophysics 318(1–4):281–302. https://doi.org/10.1016/s0040-1951(99)00316-9
González-Ruiz N, Ramírez-Pulido J, Genoways HH (2007) Review of the harvest mice (Genus Reithrodontomys) in the Mexican state of Mexico. West N Am Nat 67(2):238–250. https://doi.org/10.3398/1527-0904(2007)67[238:ROTHMG]2.0.CO;2
Hardy D, González-Cozatl F, Arellano E, Rogers D (2013) Molecular phylogeographic structure and phylogenetics of Sumichrast’s harvest mouse (Reithrodontomys sumichrasti: Family Cricetidae) based on mitochondrial and nuclear sequences. Mol Phylogenet Evol 68(2):282–292. https://doi.org/10.1016/j.ympev.2013.03.028
Harris D, Rogers DS, Sullivan J (2000) Phylogeography of Peromyscus furvus (Rodentia; Muridae) based on cytochrome b sequence data. Mol Ecol 9(12):2129–2135. https://doi.org/10.1046/j.1365-294x.2000.01135.x
Hasenaka T, Ban M, Delgado-Granados H (1994) Contrasting vulcanism in the Michoacán-Guanajuato Volcanic Field, central Mexico: shield volcanoes vs cinder cones. Geofís Int 33(1):125–138
Hillis DM, Moritz G, Mable BK (1996) Molecular Systematics (2nd Ed.). Sinauer, Sunderland, Massachsetts
Hooper ET (1952) A systematic review of the harvest mice (genus Reithrodontomys) of Latin America. Misc Publ Mus Zool Univ Mich 77:1–225.
Howell AH (1914) Revision of the American harvest mice (genus Reithrodontomys). N Am Fauna 36:1–97.
Ibarra-Arzave G, Solleiro-Rebolledo E, Sedov S, Leonard D (2019). The role of pedogenesis in palaeosols of Mexico basin and its implication in the paleoenvironmental reconstruction. Quat Int 502:267–279. https://doi.org/10.1016/j.quaint.2019.01.012
Jiménez-Noriega PMS, Terrazas T, López-Mata L, Sánchez-González A, Vibrans H (2017) Anatomical variation of five plant species along an elevation gradient in Mexico City basin within the Trans-Mexican Volcanic Belt, Mexico. J Mt Sci 14(11):2182–2199. https://doi.org/10.1007/s11629-017-4442-8
Jones G L (2017) Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J Math Biol 74:447–467. https://doi.org/10.1007/s00285-016-1034-0
Jones GL, Aydin Z, Oxelman B (2015) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31(7):991–998. https://doi.org/10.1093/bioinformatics/btu770
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29(6):1695–1701. https://doi.org/10.1093/molbev/mss020
Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30(22):3276–3278. https://doi.org/10.1093/bioinformatics/btu531.
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116. https://doi.org/10.1111/2041-210X.12410
León-Paniagua L, Navarro-Sigüenza AG, Hernández-Baños BE, Morales JC (2007) Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Mol Phylogenet Evol 42(3):653–664. https://doi.org/10.1016/j.ympev.2006.08.019
León-Tapia MA, Cervantes FA (2019) Noteworthy records and ecological niche modeling of the rare and endangered Goldman’s diminutive woodrat Nelsonia goldmani (Rodentia: Cricetidae) endemic to central Mexican highlands. Mammalia 83(4):330–342. https://doi.org/10.1515/mammalia-2018-0023
León-Tapia MA, Cervantes FA (2021) Systematics and the unexpected high mitochondrial genetic divergence of Nelsonia goldmani (Rodentia: Cricetidae) from Mexican highlands. J Mamm Evol 28:939–951. https://doi.org/10.1007/s10914-020-09532-7
León-Tapia MA, Fernández JA, Rico Y, Cervantes FA, Espinosa de los Monteros A. (2020) A new mouse of the Peromyscus maniculatus species complex (Cricetidae) from the highlands of central Mexico. J Mammal 101(4):1117–1132. https://doi.org/10.1093/jmammal/gyaa027
León-Tapia MA, Rico Y, Fernández JA, Arellano E, Espinosa de los Monteros A. (2021) Role of Pleistocene climatic oscillations on genetic differentiation and evolutionary history of the Transvolcanic deer mouse Peromyscus hylocetes (Rodentia: Cricetidae) throughout the Mexican central highlands. J Zool Syst Evol Res 59(8):2481–2499. https://doi.org/10.1007/10.1111/jzs.12541
Lounejeva-Baturina E, Morales-Puente P, Cabadas-Báez HV, Cienfuegos-Alvarado E, Vallejo-Gómez E, Solleiro-Rebolledo E (2006) Late Pleistocene to Holocene environmental changes from δ13C determinations in soils at Teotihuacan, Mexico. Geofis Int 45(2):85–98.
Macías JL, Arce JL, García-Tenorio F, Layer PW, Rueda H, Reyes-Agustin G et al (2012) Geology and geochronology of Tlaloc, Telapón, Iztaccíhuatl, and Popocatépetl volcanoes, Sierra Nevada, central Mexico. In: Aranda-Gómez JJ, Tolson G, Molina-Garza RS (eds) The Southern Cordillera and Beyond. Geological Society of America, Boulder, Colorado, pp 163–193 https://doi.org/10.1130/2012.0025(08)
Merriam CH (1901) Descriptions of 23 new harvest mice (genus Reithrodontomys). Proc Wash Acad Sci 3:547–558.
Morrone JJ (2005) Hacia una síntesis biogeográfica de México. Rev Mex Biodivers 76(2):207–252
Morrone JJ (2010) Fundamental biogeographic patterns across the Mexican Transition Zone: an evolutionary approach. Ecography 33(2):355–361. https://doi.org/10.1111/j.1600-0587.2010.06266.x
Musser GG, Carleton MD (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: A Taxonomic and Geographic Reference. The Johns Hopkins University Press, Baltimore, pp 894–1531
Nava-García E (2004) Filogeografía del ratón de los volcanes Neotomodon alstoni. Dissertation, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos
Nava-García E, Guerrero-Enríquez JA, Arellano E (2016) Molecular phylogeography of harvest mice (Reithrodontomys megalotis) based on cytochrome b DNA sequences. J Mamm Evol 23(3):297–307. https://doi.org/10.1007/s10914-015-9318-5
Ortega B, Vázquez G, Caballero M, Israde I, Lozano-García S, Schaaf P, Torres E (2010) Late Pleistocene: Holocene record of environmental changes in Lake Zirahuen, Central Mexico. J Paleolimnol 44(3):745–760. https://doi.org/10.1007/s10933-010-9449-x
Ortega-Guerrero B, Avendaño D, Caballero M, Lozano-García S, Brown ET, Rodríguez A, et al (2020) Climatic control on magnetic mineralogy during the late MIS 6 - Early MIS 3 in Lake Chalco, central Mexico. Quat Sci Rev 230:106–163. https://doi.org/10.1016/j.quascirev.2020.106163
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Pérez-Crespo MJ, Ornelas JF, González-Rodríguez A, Ruiz-Sanchez E, Vásquez-Aguilar AA, Ramírez-Barahona S (2017) Phylogeography and population differentiation in the Psittacanthus calyculatus (Loranthaceae) mistletoe: a complex scenario of climate-volcanism interaction along the Trans-Mexican Volcanic Belt. J Biogeogr 44(11):2501–2514. https://doi.org/10.1111/jbi.13070
Ramamoorthy TP, Bye R, Lot A, Fa J (1998) Diversidad Biológica de México: Orígenes y Distribución. México, Instituto de Biología, Universidad Nacional Autónoma de México, México, DF
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rodríguez-Gómez F, Oyama K, Ochoa-Orozco M, Mendoza-Cuenca L, Gaytán-Legaria R, González-Rodríguez A (2018) Phylogeography and climate-associated morphological variation in the endemic white oak Quercus deserticola (Fagaceae) along the Trans-Mexican Volcanic Belt. Botany 96(2):121–133. https://doi.org/10.1139/cjb-2017-0116
Rogers DS, Engstrom MD (1992) Evolutionary implications of allozymic variation in tropical Peromyscus of the mexicanus species group. J Mammal 73(1):55–69. https://doi.org/10.2307/1381866
Román-Colín C (2015) Estructura y variación genética en poblaciones de Neotomodon alstoni. Dissertation, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos.
Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Ruiz-Guajardo JC (2002) Filogeografía del roedor múrido endémico al Eje Volcánico Transversal: Reithrodontomys chrysopsis. Dissertation, Universidad Nacional Autónoma de México, UNAM.
Ruiz-Sanchez E, Specht CD (2013) Influence of the geological history of the Trans-Mexican Volcanic Belt on the diversification of Nolina parviflora (Asparagaceae: Nolinoideae). J Biogeogr 40(7):1336–1347. https://doi.org/10.1111/jbi.12073
Smith MF, Patton JL (1993) The diversification of South American rodents: Evidence from mitochondrial sequence data for the Akodontine tribe. Biol J Linn Soc 50(3):149–177. https://doi.org/10.1006/bijl.1993.1052
Stamatakis A (2014) RAxML Version 8. A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Sullivan J, Arellano E, Rogers DS (2000) Comparative phylogeography of Mesoamerican highland rodents: concerted versus independent responses to past climate fluctuations. Am Nat 155(6):755–768. https://doi.org/10.1086/303362
Sunny A, González-Fernández A, D’Addario M (2017) Potential distribution of the endemic imbricate alligator lizard (Barisia imbricata imbricata) in highlands of central Mexico. Amphib-Reptil 38(2):225–231. https://doi.org/10.1163/15685381-00003092
Sunny A, Duarte-de Jesús L, Aguilera-Hernández A, Ramírez-Corona F, Suárez-Atilano M, Percino-Daniel R et al (2019). Genetic diversity and demography of the critically endangered Roberts’ false brook salamander (Pseudoeurycea robertsi) in Central Mexico. Genetica 147:149–164. https://doi.org/10.1007/s10709-019-00058-2
Velo-Antón G, Parra JL, Parra-Olea G, Zamudio KR (2013) Tracking climate change in a dispersal-limited species: reduced spatial and genetic connectivity in a montane salamander. Mol Ecol 22(12):3261–3278. https://doi.org/10.1111/mec.12310
Wickliffe JK, Hoffmann FG, Carroll DS, Duninia-Barkovskaya Y, Bradley RD (2003) PCR and sequencing primers for intron 7 (Fgb-I7) of the fibrinogen, B beta polypeptide (Fgb) in mammals: a novel nuclear DNA phylogenetic marker. Occas Pap Mus Tex Tech Univ 219:1–6.
Acknowledgements
We thank Francisco X. González Cózatl at the Colección de Mamíferos, the Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos and Yolanda Hortelano Moncada at the Colección Nacional de Mamíferos (CNMA), Universidad Nacional Autónoma de México for providing tissue samples.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study’s conception and design. Data collection was performed by all authors and analyses were performed by EAA, ENG, and MALT. The first draft of the manuscript was written by EAA, ENG, and MALT. All authors commented on previous versions of the manuscript and approved the final manuscript.
Corresponding author
Ethics declarations
Financial interest
The authors have no relevant financial or non-financial interests to disclose.
Conflict of interest
The authors declare that they have no conflicts of interest or competing interests.
Competing interests
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
León-Tapia, M.Á., Nava-García, E., Cervantes, F.A. et al. Phylogeographic relationships, structure, and genetic diversity of the Mexican endemic volcano Harvest Mouse Reithrodontomys chrysopsis (Rodentia, Cricetidae). J Mammal Evol 30, 735–746 (2023). https://doi.org/10.1007/s10914-023-09670-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10914-023-09670-8