therya_19-883_CN

THERYA, 2019, Vol. 10 (3): 309-318 DOI: 10.12933/therya-19-883 ISSN 2007-3364

Genetic relationships of Caribbean lowland spiny pocket mice (Heteromys desmarestianus: Rodentia; Heteromyidae): evidence of a distinct mitochondrial lineage

Andrea Romero1*, Mark E. Mort2, J. Andrew DeWoody3, and Robert M. Timm2

1 Department of Biological Sciences and Department of Geography, Geology, and Environmental Science, University of Wisconsin-Whitewater. 800 W Main St. Whitewater, WI 53190 U.S.A. Email: romeroa@gmail.com (AR).

2 Department of Ecology and Evolutionary Biology, University of Kansas. 1450 Jayhawk Blvd., Lawrence, KS 66045 U.S.A. Email: memort@ku.edu (MEM), btimm@ku.edu (RMT).

3 Department of Biological Science and Department of Forestry & Natural Resources, Purdue University. 610 Purdue Mall, West Lafayette, IN 47907 U.S.A. Email: dewoody@purdue.edu (JAD).

*Corresponding author

Genetic studies provide important insights into the evolutionary history and taxonomy of species, allowing us to identify lineages difficult to distinguish morphologically. The relationships among species in the genus Heteromys have been in flux as new species have been described, and candidate species have been suggested in the H. desmarestianus group. One new potential species may be in Costa Rica’s Caribbean lowlands. Herein, we test the phylogenetic relationships of individuals from Costa Rica’s Caribbean lowlands to individuals from throughout the species’ range using mitochondrial sequences from cytochrome-b (cytb). We captured 116 individuals from the lowlands, sequenced their cytb gene, and incorporated 74 GenBank sequences from throughout the species’ range to test if individuals from Costa Rica’s Caribbean lowlands potentially constitute an undescribed species. Our results document a distinct mitochondrial lineage in the Caribbean lowlands of Costa Rica. Our results from extensive sampling within the lowlands show a unique mitochondrial DNA lineage, which suggests the presence of an undescribed species. The Caribbean lowlands of Costa Rica may hold other cryptic diversity, and further phylogenetic studies should incorporate samples from this area, as it may have a unique evolutionary history.

Los estudios genéticos proporcionan información importante sobre la historia evolutiva y la taxonomía de las especies, lo que nos permite identificar linajes difíciles de distinguir morfológicamente. Las relaciones filogenéticas entre las especies del género Heteromys han estado cambiando a medida que se han descrito nuevas especies y se han sugerido especies candidatas en el grupo H. desmarestianus. Una nueva especie potencial podría encontrarse en las tierras bajas del Caribe de Costa Rica. En este trabajo analizamos las relaciones filogenéticas entre individuos de las tierras bajas del Caribe de Costa Rica con individuos de todo el rango de la especie utilizando secuencias mitocondriales del citocromo-b (cytb). Capturamos 116 individuos de las tierras bajas, secuenciamos su gen cytb e incorporamos 74 secuencias GenBank de todo el área de distribución de la especie para probar si los individuos de las tierras bajas del Caribe de Costa Rica constituyen potencialmente una especie no descrita. Nuestros resultados indican la presencia de un linaje distinto basado en el ADN mitocondrial, que sugiere que los individuos de las tierras bajas del Caribe de Costa Rica probablemente son una especie distinta. Las tierras bajas del Caribe de Costa Rica pueden tener una diversidad críptica significativa. Por ello sugerimos que estudios filogenéticos adicionales deberían incorporar muestras de esta área, ya que puede tener una historia evolutiva única.

Key words: Central America; cryptic species; cytochrome b; Heteromyidae; species boundaries.

© 2019 Asociación Mexicana de Mastozoología, www.mastozoologiamexicana.org

Introduction

Understanding the relationships among evolutionary lineages is critical to estimating species diversity at varying spatial scales, reconstructing the evolutionary history of taxa, delineating ecological communities, and in making informed conservation decisions (Crozier 1992; Faith 1992; Crandall et al. 2000; Sinclair et al. 2005; Chave et al. 2007). Molecular data are increasingly used for evaluating relationships among species, identifying potential species-level clades, and identifying so-called cryptic species and thus can have significant impact on our understanding of evolutionary relationships (Sinclair et al. 2005; Beheregaray and Caccone 2007; Bickford et al. 2007; Mort et al. 2015).

With the continual improvement of molecular techniques and analyses, and broader sampling of natural populations, our understanding of phylogenetic relationships is often in flux. A group that has proven particularly difficult to delineate with traditional morphological characters are the species of spiny pocket mice of the genus Heteromys (Rodentia: Heteromyidae; see Anderson 2015 and references therein). Goldman (1911), in the first revision of the genus, recognized 13 species of Heteromys dividing them into two subgenera: Heteromys containing 12 species and Xylomys with a single species. This author further recognized the subgenus Heteromys as comprising two distinct species groups with the H. desmarestianus group containing eight species, including the first named Heteromys and most widely distributed species, H. desmarestianus (Gray, 1868). Recent research based on mitochondrial DNA indicates, however, that the lowland dry forest spiny pocket mice that were long recognized as a separate and sister genus, Liomys, are paraphyletic with respect to the species of Heteromys, thus should either be recognized as species of Heteromys or as another generic level clade (see Anderson et al. 2006; Hafner et al. 2007; Anderson and Gutiérrez 2009; and references therein). The current trend is to consider all species as belonging in the genus Heteromys.

Heteromys desmarestianus has remained a recognized taxon through several revisions (Hall 1981; Rogers and Schmidly 1982; Williams et al. 1993; Patton 2005; Rogers and González 2010), although new species have since been recognized (Anderson and Jarrín-V 2002; Anderson 2003; Anderson and Timm 2006; Anderson and Jansa 2007; Anderson and Gutiérrez 2009). Recently, Rogers and González (2010) suggested four additional clades within H. desmarestianus should be recognized. This research focuses on one of those four proposed clades that is located within the Caribbean lowlands of Costa Rica.

Heteromys desmarestianus, as currently defined, is common and widespread, ranging from southern Mexico to Colombia (Reid 2009). This species is found in evergreen and semideciduous forests, from sea level to high elevation cloud forests (Timm et al. 1989; Reid 2009). In Central America’s Caribbean lowlands, the forest spiny pocket mouse is difficult to study because populations are often found at low densities (Fleming 1974; Timm et al. 1989), and anthropogenic disturbances often have negative impacts on density and species diversity (Romero, pers. obs.). Based on molecular evidence from mitochondrial and nuclear DNA of three individuals from Caribbean lowlands of Costa Rica, Rogers and González (2010) suggested that these individuals may actually represent a separate species from what is recognized as H. desmarestianus. Herein, we test across multiple sites in the lowlands, if individuals from the Caribbean lowlands of Costa Rica are genetically distinct from what is recognized as H. desmarestianus and how this population(s) and others of the H. desmarestianus species complex are related to each other. In order to build a better understanding of the species diversity in this lineage and to test the hypothesis that there is greater diversity than is currently recognized we, herein, evaluate the relationship within the lineage currently recognized as the species H. desmarestianus.

Materials and methods

We trapped mice in several locations throughout the Caribbean lowlands of Costa Rica from 2007–2010 (Figure 1, Table 1). The Caribbean lowlands have similar ambient temperature throughout, but annual precipitation can vary from 2,400 to 4,800 mm per year (McClearn et al. 2016). Our localities (Table 1) ranged in elevation and size of forested area; our individuals from the highest elevation were from the Berlin property (Destierro) ranging from 210 to 280 masl. Samples from Berlin also represented our southern-most sample. Our northern-most samples were from the Refugio Nacional de Vida Silvestre Mixto Maquenque, close to the Costa Rica–Nicaragua border on the Río San Juan (Figure 1).

We used Sherman live traps (8 cm × 9 cm × 23 cm; H. B. Sherman Traps, Inc., Tallahassee, FL) placed at ground level and baited with cracked corn, oats, and mixed bird seed. Traps were checked daily, and when an individual was caught, a toe was removed with surgical scissors and immediately placed in 95 % ethanol. All vials with tissue and ethanol were stored frozen within hours of collection. Voucher specimens of both complete specimens and toe samples are deposited at the University of Kansas Natural History Museum, Lawrence, Kansas. This project was undertaken with the approval of the University of Kansas Institutional Animal Care and Use Committee. All animal handling protocols were in accordance with the guidelines of the American Society of Mammalogists (Sikes et al. 2016).

Laboratory procedures—116 samples from 10 sites in the Caribbean lowlands were used (Table 1) for genetic comparisons. Tissues were soaked in deionized water for one hr prior to beginning the digestion process. Standard digestion and DNA extraction were conducted following the protocol for mouse tails in Sambrook et al. (1989). The mitochondrial cytochrome-b (cytb) gene was amplified in full using the primers 765 and 766 (Bickham et al. 2004). Polymerase chain reaction (PCR) was performed using 50 μl reactions of the following reagents: 5 μl of 10× buffer, 5 μl of 10× MgCl2, 5 μl of 10× solution of dNTP, 0.5 μl of Taq DNA polymerase, 5 μl of a 10× solution of each primer, 25 μl of deionized water, and 1–2 μl of extracted DNA. Thermal cycle conditions consisted of initial heating at 94°C for 3 min, then 36 cycles of denaturation at 94°C for 30 s, annealing at 50°C for 30 s, and extension at 70°C for 2.5 min. PCR products were purified using the QiAquick PCR purification kit (Qiagen, Valencia, CA) and were subsequently used in standard sequencing reactions using Big Dye version 3.0 (Applied Biosystems, Foster City, CA). Sequencing reactions were cleaned using Sephadex spin columns and analyzed with an ABI 3100 automated genetic analyzer (Applied Biosystems, Forster City, CA). Sequence data were manually aligned using Sequencher v. 4.9 (Gene Codes Corporation, Ann Arbor, MI). We used the complete cytb gene, and all flanking regions were discarded prior to phylogenetic analysis.

To expand our dataset, we used cytb sequences of H. desmarestianus available from GenBank (Benson et al. 2013). We incorporated 74 individuals representing samples from throughout the range of the species, including specimens from near the type locality of H. desmarestianus, Cobán, Guatemala. Heteromys anomalus, H. australis, and H. nelsoni were used as outgroups (Appendix 1). We aligned all sequences with Muscle v.3.8.31 (Edgar 2004) implemented in Jalview 2.8 (Waterhouse et al. 2009).

Phylogenetic analysis—Phylogenetic relationships were obtained by performing a maximum likelihood (ML) analysis. We estimated models of molecular evolution using jModelTest v.2.1.1 with the corrected Akaike information criterion test (Guindon and Gascuel 2003; Darriba et al. 2012). We used GARLI v. 2.0 (Zwickl 2006) for ML analyses, using two independent search runs, with a maximum of five million generations each. Support values were calculated using bootstrap with 500 replications in GARLI, and results visualized and edited in FigTree v.1.4 (Rambaut 2007).

Results

The aligned data set comprises 1,142 characters of which 738 were constant, 335 characters were parsimony-informative, and 69 variable characters were parsimony-uninformative. The model of DNA substitution inferred from jModeltest 2.1.1 is TIM2+I+G.

The ML tree topology (Figure 2) shows two highly supported lineages for all individuals currently considered H. desmarestianus. One clade comprises all samples from the Caribbean lowlands of Costa Rica and had very strong (99 %) bootstrap support. The other lineage comprises all of the H. desmarestianus sequences obtained from Belize, Costa Rica (in part), El Salvador, Guatemala, Honduras, México, and Nicaragua and also have strong bootstrap support (83%). Within the clade containing samples from the Caribbean lowlands of Costa Rica (not shown in Figure 2), the individuals from two sites, Berlin and Maquenque, formed clades supported by strong bootstrap support (90 % and 86 %, respectively). Two individuals from the eight sampled at Maquenque were placed elsewhere within the tree, and thus the nonexclusive nature of the branching pattern complicates lower level population patterns from these data. Maquenque is biologically quite interesting being in the floodplain of the Río San Juan and our continued studies there are elucidating other unexpected patterns with other rodent species.

Specimens collected near Baja Verapas, Guatemala (GU646966, GU646967, GU646968; Appendix) ~30 km from the type locality, Cobán, cluster with specimens from Belize, El Salvador, Honduras, and parts of México, but not with specimens from the Caribbean lowlands of Costa Rica (Figure 2). The specimen that clustered closest to Cobán from our Costa Rican lowland dataset was from the Costa Rica–Nicaragua border region ~ 850 km away. Genbank accession numbers of new sequences are reported in the Appendix.

Discussion

The results of this study strongly support the hypothesis that what is currently called Heteromys desmarestianus in Central America and northern-most South America comprises two very distinct clades, one being found in the Caribbean lowlands of Costa Rica and the other comprising all other populations. Our results show a clear geographic pattern; individuals currently considered H. desmarestianus in the Caribbean lowlands of Costa Rica harbor distinct mtDNA haplotypes from individuals considered H. desmarestianus found elsewhere in the Neotropics, including other areas in Costa Rica (Figure 2). The specimens from near the type locality of H. desmarestianus, Cobán, Guatemala form a well-supported clade with specimens from southern México, Belize, El Salvador, and Honduras. Specimens from western Costa Rica and one specimen from western Nicaragua all form another distinct clade.

Costa Rica is only ~51,000 km2, yet its variable topography and climate result in diverse habitats with unique flora and fauna (Janzen 1983). Currently, four main mountain ranges divide the country into the Pacific and Caribbean sides. These mountain ranges span southeast to northwest, and are of diverse ages and origins (Anderson and Timm 2006). Extending from western Panama to northern Costa Rica, the Cordillera de Talamanca, Cordillera Central, and Cordillera de Tilarán form an expansive mountain range with peak elevations of over 3,000, 2,500, and 2,000 masl, respectively. The Cordillera de Guanacaste is the northernmost range in Costa Rica, and is comprised of several isolated volcanoes, with passes of ~500 to 700 masl in elevation that connect the Pacific and Caribbean sides (Anderson and Timm 2006). The historical and current topography of these mountain ranges probably shaped the diversification and speciation patterns in the flora and fauna observable today.

The family Heteromyidae originated on the North America continent (Wood 1935; Schmidly et al. 1993), and fossil remains for the subfamily Heteromyinae are known from the Pliocene, Pleistocene, and Holocene (Rogers 1990). Rogers (1990) estimated that the major groups within this subfamily diverged ~12 to 13 mya, yet the historical events that produced the H. desmarestianus group are largely unknown. The geologic history of the Caribbean, and Central and South America has been a debated topic (Bartoli et al. 2005; Montes et al. 2012a, 2012b, 2015; Bacon et al. 2015; O’Dea et al. 2016), but it is thought that islands of volcanic origin between Central and South America may have allowed faunal exchanges prior to the formation of a permanent land bridge (Bartoli et al. 2005; Woodburne 2010; O’Dea et al. 2016). The time of the emergence of a permanent Panamanian land bridge is disputed, and estimates range from 2 to 7 mya (Montes et al. 2012b; but see Bacon et al. 2015). Because of the widespread distribution pattern of the H. desmarestianus group, a hypothesis similar to the one suggested for other rodent groups has been proposed for this clade (Patterson and Pasqual 1972; Baskin 1978; Simpson 1980; Rogers 1990; Almendra and Rogers 2012; Pine et al. 2012); It is thought that considerable radiation occurred in the Miocene and Pliocene throughout Central America, with a subsequent entry to South America via the Panamanian land bridge (Rogers 1990; Schmidly et al. 1993).

Our results herein document a broad distribution of this distinct and unrecognized Costa Rican lowland lineage. The northern-most samples within this clade are from the Costa Rica–Nicaraguan border, while the southern-most are ~86 km southeast of there. Unfortunately, little is known about spiny pocket mice in the lowlands of Nicaragua and southern Costa Rica, and we are unable to demarcate northern and southern boundaries of this mtDNA lineage. In terms of elevation, the lowland specimens came from forests that ranged in elevation from ~22 to 280 masl. In our analysis, we included a single GenBank sequence from Cerro Honduras in Parque Nacional Braulio Carrillo. The park, along with privately owned reserves and biological stations, is part of a continuously forested transect that expands from the lowlands at La Selva Biological Station and reaches elevations > 2,700 masl. Although we do not have specific data on the elevation from which this particular specimen came, our results do show that this higher elevation specimen is a member of the clade with H. desmarestianus proper from throughout Central America and does not group with our samples from the lowlands, including specimens from the nearby La Selva Biological Station. While our results suggest two distinct clades, we are unable to delineate at this time limits of their specific elevational range, or if there are areas of overlap or hybridization that await discovery.

Our results expand upon, compliment, and confirm Rogers and González (2010), who used both cytb and nuclear data, and identified three individuals from the Caribbean lowlands of Costa Rica as a potential candidate species. Although useful to characterize species that are difficult to establish based on morphological data, DNA sequence data do have limitations, particularly when a single marker is used (Farias et al. 2001; Rogers and González 2010). Now that we provide more extensive sampling of individuals from the Caribbean lowlands of Costa Rica, we recommend that future studies determine if population structure based on nuclear markers correlates with the distinctive mtDNA lineage of the Costa Rican lowland. Further investigation focused on nuclear DNA is also important because mitochondrial DNA and nuclear DNA can be discordant (Lack et al. 2010, Bernardo et al. 2019). This can result in distinct mitochondrial DNA lineages within a population or species that are not supported by nuclear DNA.

The diversity of rodent communities in the Caribbean lowlands of Costa Rica have been vastly understudied and we believe underestimated, in part, because of low densities resulting in low trap success (Romero, pers. obs.). Consequently, the lack of data and specimens has hindered our understanding of the basic phylogenetic relationships and biogeographic patterns of species in the area. Other widespread rodent species have been found to hold similar patterns reported herein, where individuals from the Caribbean lowlands of Costa Rica are genetically distinct and potentially new species (Timm, unpublished data). These data suggest that there may be significant cryptic diversity in the lowlands, and that more phylogenetic studies should include samples from this region to identify potential biogeographic patterns for rodents in the Neotropics. This information is necessary not only to understand phylogenetic relationships, but also to have a grasp on the patterns and levels of diversity for the area, and make large-scale conservation decisions based on this information. We believe that our results, in conjunction with future studies that aim to identify and delineate diversity in the H. desmarestianus species complex, and the relationships between these species, will allow for a greater understanding of the historical events leading to speciation in this group.

Clearly much remains to be learned about the diversity of these widespread and common rodents that are considered keystone species in the Neotropics.

Acknowledgments

We thank D. McClearn, the Organization for Tropical Studies, and all of the landowners who supported our research. MINAET–SINAC and J. Guevara provided research permits. V. Weigand Noble, G. Fandos, and R. Garcia provided expert assistance in the field often under trying conditions. We thank A. Rinner, N. Marra, J. C. Patton, and O. F. Toro for generously sharing their expertise and support. Darrin Lunde, Suzanne Peurach, and Neal Woodman made specimens housed in the United States National Museum of Natural History, Washington, D. C. available to us and work in the collections productive.

Literature Cited

Almendra, A. L., and D. S. Rogers. 2012. Biogeography of Central American mammal: patterns and processes. Pp. 203–229 in Bones, clones, and biomes: the history and geography of Recent Neotropical mammals (Patterson, B. D., and L. P. Costa, eds.). University of Chicago Press. Chicago, U.S.A.

Anderson, R. P. 2003. Taxonomy, distribution, and natural history of the genus Heteromys (Rodentia: Heteromyidae) in western Venezuela, with the description of a dwarf species from the Península de Paraguaná. American Museum Novitates 3396:1–43.

Anderson, R. P. 2015. Family Heteromyidae. Pp. 51–58 in Mammals of South America, Volume 2: Rodents (Patton, J. L., U. F. J. Pardiñas, and G. D’Elía, eds.). University of Chicago Press. Chicago, U.S.A.

Anderson, R. P., and E. E. Gutiérrez. 2009. Taxonomy, distribution, and natural history of the genus Heteromys (Rodentia: Heteromyidae) in central and eastern Venezuela, with the description of a new species from the Cordillera de la Costa. Pp. 33–93 in Systematic mammalogy: contributions in honor of Guy G. Musser. (Voss, R. S., and M. D. Carleton, eds.). Bulletin of the American Museum of Natural History 331.

Anderson, R. P., and S. A. Jansa. 2007. Genetic comparisons between Heteromys desmarestianus and the recently described H. nubicolens (Rodentia: Heteromyidae) in northwestern Costa Rica. Mammalian Biology 72:54–61.

Anderson, R. P., and P. Jarrín-V. 2002. A new species of spiny pocket mouse (Heteromyidae: Heteromys) endemic to western Ecuador. American Museum Novitates 3382:1–26.

Anderson, R. P., and R. M. Timm. 2006. A new montane species of spiny pocket mouse (Heteromyidae: Heteromys) from northwestern Costa Rica. American Museum Novitates 3509:1–38.

Anderson, R. P., M. Weksler, and D. S. Rogers. 2006. Phylogenetic analyses of spiny pocket mice (Heteromyidae: Heteromyinae) based on allozymic and morphological data. Journal of Mammalogy 87:1218–1233.

Bacon, C. D., D. Silvestro, C. Jaramillo, B. T. Smith, P. Chakrabarty, and A. Antonelli. 2015. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the National Academy of Sciences 112:6110–6115.

Bartoli, G., M. Sarthein, M. Weinelt, H. Erlenkeuser, D. Garbe-Schönberg, and D. W. Lea. 2005. Final closure of Panama and the onset of northern hemisphere glaciation. Earth and Planetary Science Letters 237:33–44.

Baskin, J. A. 1978. Bensonomys, Calomys, and the origin of the phyllotine group of Neotropical cricetines (Rodentia: Cricetidae). Journal of Mammalogy 59:125–135.

Beheregaray, L. B., and A. Caccone. 2007. Cryptic biodiversity in a changing world. Journal of Biology 6:9.1–9.5.

Benson, D. A., M. Cavanaugh, K. Clark, I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and E. W. Sayers. 2013. GenBank. Nucleic Acids Research 41:36–42.

Bernardo, P. H., et al. 2019. Extreme mito-nuclear discordance in a peninsular lizard: the role of drift, selection, and climate. Heredity: 1.

Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. Ng, R. Meier, K. Winker, K. K. Ingram, and I. Das. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22:148–155.

Bickham, J. W., J. C. Patton, D. A. Schlitter, I. L. Rautenbach, and R. L. Honeycutt. 2004. Molecular phylogenetics, karyotypic diversity, and partition of the genus Myotis (Chiroptera: Vespertilionidae). Molecular Phylogenetics and Evolution 33:333–338.

Chave, J., G. Chust, and C. Thébaud. 2007. The importance of phylogenetic structure in biodiversity studies. Pp. 150–167 in Scaling biodiversity (Storch, D., P. L. Marquet, and J. H. Brown, eds.). Cambridge University Press. Cambridge, U.K.

Crandall, K. A., O. R. P. Bininda-Emonds, G. M. Mace, and R. K. Wayne. 2000. Considering evolutionary processes in conservation biology. TREE 15:290–295.

Crozier, R. H. 1992. Genetic diversity and the agony of choice. Biological Conservation 61:11–15.

Darriba, D., G. L. Taboada, R. Doallo, and D. Posada. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.

Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797.

Faith, D. P. 1992. Conservation evaluation and phylogenetic diversity. Biological Conservation 61:1–10.

Farias, I. P., G. Ortí, I. Sampaio, H. Schneider, and A. Meyer. 2001. The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. Journal of Molecular Evolution 53:89–103.

Fleming, T. H. 1974. The population ecology of two species of Costa Rican heteromyid rodents. Ecology 55:493–510.

Goldman, E. A. 1911. Revision of the spiny pocket mice (genera Heteromys and Liomys). North American Fauna 34:1–70.

Gray, J. E. 1868. Synopsis of the species of Saccomyinae, or pouched mice in the collection of the British Museum. Proceedings of the Zoological Society of London 1868:199–206.

Guindon, S., and O. Gascuel. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52:696–704.

Hafner, J. C., J. E. Light, D. J. Hafner, M. S. Hafner, E. Reddington, D. S. Rogers, and B. R. Riddle. 2007. Basal clades and molecular systematics of heteromyid rodents. Journal of Mammalogy 88:1129–1145.

Hall, E. R. 1981. The mammals of North America. John Wiley & Sons, Inc. New York, U.S.A.

Janzen, D. H. 1983. Costa Rican natural history. University of Chicago Press. Chicago, U.S.A.

Lack, J. B., J. E. Wilkinson, and R. A. Van Den Bussche. 2010. Range-wide population genetic structure of the pallid bat (Antrozous pallidus)—incongruent results from nuclear and mitochondrial DNA. Acta Chiropterologica 12:401–413.

McClearn, D., et al. 2016. The Caribbean lowland evergreen moist and wet forests. Pp. 527–587 in Costa Rican ecosystems (M. Kappelle, ed.). University of Chicago Press. Chicago, U.S.A.

Montes, C., et al. 2012a. Arc-continent collision and orocline formation: closing of the Central American seaway. Journal of Geophysical Research: Solid Earth 117(B4):1–25.

Montes, C., et al. 2012b. Evidence for middle Eocene and younger land emergence in central Panama: implications for isthmus closure. Bulletin of the Geological Society of America 124:780–799.

Montes, C., et al. 2015. Middle Miocene closure of the Central American Seaway. Science 348(6231):226–229.

Mort, M. E., et al. 2015. Multiplexed-shotgun-genotyping data resolve phylogeny within a very recently derived insular lineage. American Journal of Botany 102:634–641.

O’Dea, A., et al. 2016. Formation of the Isthmus of Panama. Science Advances 2(e1600883):1–11.

Patterson, B., and R. Pascual. 1972. The fossil mammal fauna of South America. Pp. 247–309 in Evolution, mammals, and southern continents (Keast, A., F. C. Erk, and B. Blass, eds.). State University of New York Press. Albany, U.S.A.

Patton, J. L. 2005. Family Heteromyidae. Pp. 844–858 in Mammal species of the world: a taxonomic and geographic reference (Wilson, D. E., and D. M. Reeder, eds.). 3rd edition. Johns Hopkins University Press. Baltimore, U.S.A.

Pine, R. H., R. M. Timm, and M. Weksler. 2012. A newly recognized clade of trans-Andean Oryzomyini (Rodentia: Cricetidae), with description of a new genus. Journal of Mammalogy 93:851–870.

Rambaut, A. 2007. FigTree. http://tree.bio.ed.ac.uk/software/figtree. Accessed 13 February 2013.

Reid, F. A. 2009. A field guide to the mammals of Central America & Southeast Mexico. 2nd edition. Oxford University Press. New York, U.S.A.

Rogers, D. S. 1990. Genic evolution, historical biogeography, and systematic relationships among spiny pocket mice (subfamily Heteromyinae). Journal of Mammalogy 71:668–685.

Rogers, D. S., and M. W. González. 2010. Phylogenetic relationships among spiny pocket mice (Heteromys) inferred from mitochondrial and nuclear sequence data. Journal of Mammalogy 91:914–930.

Rogers, D. S., and D. J. Schmidly. 1982. Systematics of spiny pocket mice (genus Heteromys) of the desmarestianus species group from México and northern Central America. Journal of Mammalogy 63:375–386.

Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd edition. Cold Spring Harbor Laboratory Press. New York, U.S.A.

Schmidly, D. J., K. T. Wilkins, and J. N. Derr. 1993. Biogeography. Pp 319–356 in Biology of the Heteromyidae (Genoways, H. H., and J. H. Brown, eds.). Special Publications 10, American Society of Mammalogists. Lawrence, U.S.A.

Sikes, R.S., et al. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688.

Simpson, G. G. 1980. Splendid isolation: the curious history of South American mammals. Yale University Press. New Haven, U.S.A.

Sinclair, E. A., M. Pérez-Losada, and K. A. Crandall. 2005. Molecular phylogenetics for conservation biology. Pp. 19–56 in Phylogeny and conservation (Purvis, A., J. L. Glittleman, and T. Brooks, eds.). Cambridge University Press. Cambridge, U.K.

Timm, R. M., D. E. Wilson, B. L. Clauson, R. K. LaVal, and C. S. Vaughan. 1989. Mammals of the La Selva–Braulio Carrillo complex, Costa Rica. North American Fauna 75:1–162.

Waterhouse, A. M., J. B. Procter, D. M. A. Martin, M. Clamp, and G. J. Barton. 2009. Jalview version 2–a multiple sequence alignments editor and analysis workbench. Bioinformatics 25:1189–1191.

Williams, D. F., H. H. Genoways, and J. K. Braun. 1993. Taxonomy. Pp. 38–196 in Biology of the Heteromyidae (Genoways, H. H., and J. H. Brown, eds.). Special Publication 10, American Society of Mammalogists. Lawrence, U.S.A.

Wood, A. E. 1935. Evolution and relationships of the heteromyid rodents with new forms from the Tertiary of western North America. Annals of Carnegie Museum 24:73–262.

Woodburne, M. O. 2010. The great American biotic interchange: dispersals, tectonics, climate, sea level and holding pens. Journal of Mammalian Evolution 17:245–264.

Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas. Austin, U.S.A.

Associated editor: Monica Díaz

Submitted: June 23, 2019; Reviewed: July 28, 2019;

Accepted: August 28, 2019; Published on line: September 16, 2019.

Appendix 1.

Localities and specimen information for samples utilized in the study. Map numbers correspond to numbers on Figure 1. Data for specimens not from the Caribbean lowlands of Costa Rica were obtained from GenBank and the published papers associated with the GenBank accession numbers.

Map

Species

Specimen information

GenBank

Locality

Country

N/A

H. anomalus

CM 78170 = MDE 2087 = AK 3468

GU646919

Miranda, 25 km N Altagracia de Orituco, 500 m

Venezuela

N/A

H. anomalus

CM 78168 = MDE 2034 = AK3437

GU646924

Sucre, 40 km NW Caripito, 250 m

Venezuela

40a

H. australis

LSUMZ 35452 = MSH 1187 = TK 22565

GU646926

Darién, approximately 6 km NW Cana, E. slope Cerro Pirre, 1,200 m

Panama

40b

H. australis

ROM 104356 = F38215

GU646927

Darién, Cerro Pirre, Parque Nacional Darién

Panama

8a

H. desmarestianus

CM 91988 = AK7663

GU646929

Stann Creek District, 3.4 km WNW Quam Bank, Cockscomb Basin

Belize

8b

H. desmarestianus

CM91980 = AK7688

GU646930

Stann Creek District, 6.8 km WNW Quam Bank, Cockscomb Basin

Belize

8c

H. desmarestianus

CM 91951 = AK 7665

GU646932

Stann Creek District, 7.7 km WNW Quam Bank, Cockscomb Basin

Belize

9a

H. desmarestianus

CM 91991 = AK 7540

GU646933

Toledo District, 1.0 km NNE Salamanca, Forestry Camp, Columbia Forest Reserve

Belize

9b

H. desmarestianus

CM 91989 = AK 7555

GU646934

Toledo District, 2.4 km NNW Salamanca, Forestry Camp, Columbia Forest Reserve

Belize

9c

H. desmarestianus

CM 91993 = AK 7588

GU646935

Toledo District; 2.1 km NNE Salamanca, Forestry Camp, Columbia Forest Reserve

Belize

9c

H. desmarestianus

CM 91994 = AK 7586

GU646936

Toledo District; 2.1 km NNE Salamanca, Forestry Camp, Columbia Forest Reserve

Belize

9c

H. desmarestianus

CM 91995 = AK 7589

GU646937

Toledo District; 2.1 km NNE Salamanca, Forestry Camp, Columbia Forest Reserve

Belize

18

H. desmarestianus

KU 158615 = MK 00-112

DQ450094

Guanacaste, Area de Conservación Guanacaste, approximately 20 km NNE Liberia, Pailas, Sendero Pailas, near Rio Colorado, 800 m

Costa Rica

17

H. desmarestianus

KU 158508 = MK 99-088

DQ450095

Guanacaste: Área de Conservación Guanacaste, ca. 39 km N Liberia, Pitilla, Sendero Orosilito

Costa Rica

17

H. desmarestianus

KU 158509 = MK 99-090

DQ450096

Guanacaste: Área de Conservación Guanacaste, ca. 39 km N Liberia, Pitilla, Sendero Orosilito

Costa Rica

17

H. desmarestianus

KU 158512 = MK 99-093

DQ450097

Guanacaste: Área de Conservación Guanacaste, ca. 39 km N Liberia, Pitilla

Costa Rica

17

H. desmarestianus

KU 158513 = MK 99-094

DQ450098

Guanacaste: Área de Conservación Guanacaste, ca. 39 km N Liberia, Pitilla

Costa Rica

17

H. desmarestianus

KU 158514 = MK 99-102

DQ450099

Guanacaste: Área de Conservación Guanacaste, ca. 39 km N Liberia, Pitilla, Sendero Carica

Costa Rica

22

H. desmarestianus

ROM 113310 = F 48617

GU646938

Alajuela; 10 km E of Sucre, Parque Nacional, Juan Costro Blanco

Costa Rica

22

H. desmarestianus

ROM 113311 = F 48618

GU646939

Alajuela; 10 km E of Sucre, Parque Nacional, Juan Costro Blanco

Costa Rica

24

H. desmarestianus

ROM 113130 = F 48436

GU646940

Cartago, Iztaru, Cerros de la Carpintera

Costa Rica

24

H. desmarestianus

ROM 113131 = F 48437

GU646941

Cartago, Iztaru, Cerros de la Carpintera

Costa Rica

27

H. desmarestianus

MVZ 164823 = DSR 2153

GU646942

Cartago, Rio Reventazón, 5.6 km SE (by road) Turrialba, 450 m

Costa Rica

27

H. desmarestianus

MVZ 164823 = DSR 2154

GU646943

Cartago, Rio Reventazón, 5.6 km SE (by road) Turrialba, 450 m

Costa Rica

27

H. desmarestianus

MVZ 164825 = DSR 2166

GU646944

Cartago, Rio Reventazón, 5.6 km SE (by road) Turrialba, 450 m

Costa Rica

27

H. desmarestianus

MVZ 164826 = DSR 2167

GU646945

Cartago, Rio Reventazón, 5.6 km SE (by road) Turrialba, 450 m

Costa Rica

27

H. desmarestianus

MVZ 164827 = DSR 2246

GU646946

Cartago, Rio Reventazón, 5.6 km SE (by road) Turrialba, 450 m

Costa Rica

26

H. desmarestianus

ROM 97324 = FAR 111

GU646947

Cartago, 4 km SE of Turrialba by road, Catie, 600 m

Costa Rica

26

H. desmarestianus

ROM 97325 = FAR 112

GU646948

Cartago, 4 km SE of Turrialba by road, Catie, 600 m

Costa Rica

20

H. desmarestianus

MVZ 164828 = DSR 2123

GU646949

Guanacaste, 4.1 km NE (by road) Tilarán, 650 m

Costa Rica

20

H. desmarestianus

MVZ 164829 = DSR 2124

GU646950

Guanacaste, 4.1 km NE (by road) Tilarán, 650 m

Costa Rica

20

H. desmarestianus

MVZ 164831 = DSR 2134

GU646952

Guanacaste, 4.1 km NE (by road) Tilarán, 650 m

Costa Rica

20

H. desmarestianus

MVZ 164833 = DSR 2124

GU646953

Guanacaste, 4.1 km NE (by road) Tilarán, 650 m

Costa Rica

20

H. desmarestianus

MVZ 164835 = DSR 2143

GU646954

Guanacaste, 4.1 km NE (by road) Tilarán, 650 m

Costa Rica

21

H. desmarestianus

MVZ 164839 = DSR 2121

GU646955

Guanacaste: 5.0 km NE (by road) Tilarán, 675 m

Costa Rica

21

H. desmarestianus

MVZ 164840 = DSR 2122

GU646956

Guanacaste: 5.0 km NE (by road) Tilarán, 675 m

Costa Rica

19

H. desmarestianus

ROM 113244 = F 48551

GU646957

Guanacaste: Volcán Santa Maria

Costa Rica

19

H. desmarestianus

ROM 113245 = F 48552

GU646958

Guanacaste: Volcán Santa Maria

Costa Rica

28

H. desmarestianus

LSUMZ 28354 = MSH 1260

GU646959

Puntarenas, 1 km N, 5 km W Palmar Norte, 33 m

Costa Rica

25

H. desmarestianus

BYU 15197 = EA 21

GU646960

San José, Bajo de Iglesia, SW Volcán Irazu, Cascajal de Coronado

Costa Rica

25

H. desmarestianus

BYU 15198 = EA 22

GU646961

San José, Bajo de Iglesia, SW Volcán Irazu, Cascajal de Coronado

Costa Rica

23

H. desmarestianus

BYU 15195 = EA 78

GU646962

San José, Parque Nacional Braulio Carillo, Moravia, Cerro Honduras

Costa Rica

23

H. desmarestianus

BYU 15196 = EA 79

GU646963

San José, Parque Nacional Braulio Carillo, Moravia, Cerro Honduras

Costa Rica

29

H. desmarestianus

No specimen available

MN335341

Alajuela: Maquenque, 10°40’48.96”N, 84°10’39.65”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335416

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335415

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335420

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335369

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335417

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335429

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335422

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335368

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

30

H. desmarestianus

No specimen available

MN335428

Heredia: Selva Verde, 10°26’46.36”N, 84°04’00.62”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335344

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335353

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335356

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335351

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335379

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335345

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335412

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335382

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335405

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335363

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335404

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335411

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335403

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335350

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335389

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335362

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335383

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335336

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335381

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335343

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335387

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335354

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335386

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335407

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335359

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335376

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335391

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335357

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335361

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335349

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335399

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335350

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335355

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335390

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335380

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335358

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335384

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335352

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335342

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335347

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335340

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

32

H. desmarestianus

No specimen available

MN335346

Heredia: La Selva Biological Station, 10°25’47.90”N, 84°00’55.15”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335392

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335378

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335395

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335364

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335371

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335365

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335367

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335338

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335337

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335394

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335372

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

33

H. desmarestianus

No specimen available

MN335385

Heredia: Tirimbina, 10°24’45.58”N, 84°07’02.55”W

Costa Rica

38

H. desmarestianus

No specimen available

MN335406

Limon Province: Berlin, 10°07’59.73”N, 83°36’18.38”W

Costa Rica

38

H. desmarestianus

No specimen available

MN335397

Limon Province: Berlin, 10°07’59.73”N, 83°36’18.38”W

Costa Rica

38

H. desmarestianus

No specimen available

MN335398

Limon Province: Berlin, 10°07’59.73”N, 83°36’18.38”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335409

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335348

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335334

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335410

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335402

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335401

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335333

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335370

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

35

H. desmarestianus

No specimen available

MN335414

Heredia: Agrícola Sofía, 10°27’32.01”N, 83°58’41.40”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335332

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335413

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335385

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335393

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335335

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335375

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335332

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335419

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335388

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335360

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335373

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

36

H. desmarestianus

No specimen available

MN335374

Heredia: Starky, 10°26’31.73”N, 83°59’09.16”W

Costa Rica

37

H. desmarestianus

No specimen available

MN335424

Heredia: 10°26’03.92”N, 84°07’42.76”W

Costa Rica

37

H. desmarestianus

No specimen available

MN335418

Heredia: 10°26’03.92”N, 84°07’42.76”W

Costa Rica

14

H. desmarestianus

ROM 101369 = F 35547

GU646964

Santa Ana, Parque Nacional Montecristi, Bosque Nebuloso, 2,200 m

El Salvador

14

H. desmarestianus

ROM 101389 = F 35567

GU646965

Santa Ana, Parque Nacional Montecristi, Bosque Nebuloso, 2,200 m

El Salvador

11

H. desmarestianus

LVT 5499

AY926358

Tikal, El Peten

Guatemala

12

H. desmarestianus

ROM 98405 = FN 31394

GU646966

Baja Verapaz: 5 km E of Puruhla, 1,550 m

Guatemala

12

H. desmarestianus

ROM 98406 = FN 31395

GU646967

Baja Verapaz: 5 km E of Puruhla, 1,550 m

Guatemala

12

H. desmarestianus

FN 31402

GU646968

Baja Verapaz: 5 km E of Puruhla, 1,550 m

Guatemala

10a

H. desmarestianus

ROM 99603 = FN 32272

GU646969

El Peten: Biotope, Cerro Cahui, El Remate

Guatemala

10a

H. desmarestianus

ROM 99604 = FN 32273

GU646970

El Peten: Biotope, Cerro Cahui, El Remate

Guatemala

10b

H. desmarestianus

ROM 99469 = FN 32318

GU646971

El Peten: Campo los Guacamayos, Biotopo Laguna del Tigre, 40 km N El Naranjo

Guatemala

11

H. desmarestianus

ROM 99292 = FN 31842

GU646973

El Peten, Tikal

Guatemala

11

H. desmarestianus

ROM 99293 = FN 31843

GU646974

El Peten, Tikal

Guatemala

13

H. desmarestianus

ROM 98266 = FN 31252

GU646975

Sacatepequez, 5 km W San Miguel Duanas, 1,765 m

Guatemala

13

H. desmarestianus

ROM 98265 = FN 31254

GU646976

Sacatepequez, 5 km W San Miguel Duanas, 1,765 m

Guatemala

15

H. desmarestianus

TCWC 52259 = BEL 865 = AK 9696

DQ168466

Atlántida, Lancetilla

Honduras

1a

H. desmarestianus

MVZ 161229 = DSR 1685

DQ168467

Oaxaca; Distrito Ixtlán, Vista Hermosa, 1,000 m

Mexico

5

H. desmarestianus

ROM 97050 = FN 30853

GU646977

Campeche, 10 km N El Refugio

Mexico

5

H. desmarestianus

ROM 97051 = FN 30854

GU646978

Campeche, 10 km N El Refugio

Mexico

6

H. desmarestianus

ROM 96089 = FN 29880

GU646979

Campeche: 25 km N Xpujil

Mexico

2

H. desmarestianus

ASNHC 3515 = LAF 1689

GU646980

Chiapas, 12 km N (by road) Berriozábal

Mexico

2

H. desmarestianus

ASNHC 1424 = ASK 660

GU646981

Chiapas, 12 km N (by road) Berriozábal

Mexico

2

H. desmarestianus

ASNHC 1425 = ASK 689

GU646982

Chiapas, 12 km N (by road) Berriozábal

Mexico

4a

H. desmarestianus

ASNHC 1426 = ASK 51

GU646983

Chiapas, 6.6 km S Palenque

Mexico

4b

H. desmarestianus

ASNHC 5826 = ASK 49

GU646984

Chiapas, 9.0 km S Palenque

Mexico

4c

H. desmarestianus

ROM 96096 = FN 29887

GU646985

Chiapas, 12.5 km S Palenque

Mexico

4c

H. desmarestianus

ROM 96105 = FN 29896

GU646986

Chiapas, 12.5 km S Palenque

Mexico

4d

H. desmarestianus

ASNHC 1440 = ASK 29

GU646987

Chiapas, 1.2 km E Ruinas de Palenque

Mexico

4d

H. desmarestianus

ASNHC 1441 = ASK 31

GU646988

Chiapas, 1.2 km E Ruinas de Palenque

Mexico

3a

H. desmarestianus

ROM 97542 = FN 33018

GU646989

Chiapas, 6 km E of Rayon, 1,560 m

Mexico

3b

H. desmarestianus

ASNHC 1431 = ASK 589

GU646990

Chiapas, 9 km SE Rayon

Mexico

3b

H. desmarestianus

ASNHC 1432 = ASK 591

GU646991

Chiapas, 9 km SE Rayon

Mexico

7

H. desmarestianus

ROM 97520 = FN 30995

GU646992

Quintana Roo, 1 km N Noh-Bec

Mexico

7

H. desmarestianus

ROM 97521 = FN 30996

GU646993

Quintana Roo, 1 km N Noh-Bec

Mexico

1b

H. desmarestianus

CM 79530 = DSR 934 = AK 3108

GU646994

Oaxaca, Vista Hermosa, 1,000 m

Mexico

1b

H. desmarestianus

MVZ 161230 = DSR 1686

GU646995

Oaxaca; Distrito Ixtlán, Vista Hermosa, 1,000 m

Mexico

16

H. desmarestianus

ROM 112284 = F 48170

GU646996

Esteli, Esteli

Nicaragua

39

H. nelsoni

BYU 20644 = DSR 7189

GU647014

Chiapas, Cerro Mozotal, 15º25.866’N, 92º20.274’W, 2,930 m

Panama

Figure 1. Map of localities for all specimens used in the study. Localities 29–38 represent specimens from Costa Rica’s Caribbean lowlands. Symbols correspond to lineages depicted in the maximum likelihood tree (Figure 2). H. anomalus from Venezuela not depicted herein. Specific data regarding localities can be obtained from Appendix 1.

Table 1. Sampling areas in the Caribbean lowlands of Costa Rica. Locality numbers refer to numbers from Figure 1.

Site (locality)

Max elevation (m)

Min elevation (m)

Latitude

Longitude

Maquenque (29)

70.1

47

10° 40 48.96 N

-84° 10 39.65 W

Water Tower (34)

98

42

10° 27 52.90 N

-84° 00 29.47 W

Agrícola Sofía (35)

68.58

51.21

10° 27 32.01 N

-83° 58 41.40 W

Juan Enriques (31)

189.59

45.72

10° 27 20.46 N

-84° 04 01.70 W

Selva Verde (30)

164.59

84.43

10° 26 46.36 N

-84° 04 00.62 W

Starky (36)

69

43

10° 26 31.73 N

-83° 59 09.16 W

Fragment A (37)

162

131

10° 2603.92 N

-84° 07 42.76 W

La Selva (32)

146

22

10° 25 47.90 N

-84° 00 55.15 W

Tirimbina (33)

224.03

149.35

10° 24 45.58 N

-84° 07 02.55 W

Berlin (38)

280

210

10° 07 59.73 N

-83° 36 18.38 W

Figure 2. Maximum likelihood tree of our Heteromys dataset, based on cytb sequences. The maximum likelihood tree is collapsed for visual clarity, and shows the results with bootstrap values. These results indicate that individuals from Costa Rica’s Caribbean lowlands harbor unique mitochondrial lineages that could reflect reproductive isolation. Symbols in tree are used in Figure 1 to show the geographic range of lineages. Tree is rooted with H. golmani.

Enlaces refback

  • No hay ningún enlace refback.


FACTOR DE IMPACTO 2020 (SCOPUS): 1.2


THERYA es publicada por la Asociación Mexicana de Mastozoología A. C.  Se distribuye bajo una Licencia de Creative Commons Atribución-NoComercial-SinDerivar 4.0 Internacional.

DERECHOS DE AUTOR Y DERECHOS CONEXOS, THERYA es una publicación digital cuatrimestral editada por la Asociación Mexicana de Mastozoología A. C.  Hacienda Vista Hermosa 107, Colonia Villa Quietud, Coyoacan 04960.  Distrito Federal, México.  Telefono (612) 123-8486, www.mastozoologiamexicana.org.  Editor responsable: Dr. Sergio Ticul Álvarez Castañeda (therya@cibnor.mx).  Reservas de Derechos al Uso Exclusivo No. 04-2009-112812171700-102, ISSN: 2007-3364 ambos otorgados por el Instituto Nacional de Derechos de Autor.  Responsable de la última actualización de este número, Unidad de informática de la Asociación Mexicana de Mastozoología A. C.  Dr. Sergio Ticul Álvarez Castañeda.  Instituto Politécnico Nacional 195.  La Paz, Baja California Sur, C. P. 23096.  Tel 612 123 8486.