Comparative Phylogeography of Oryzomys Couesi and Ototylo

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thesis abstract ISSN 1948‐6596 Comparative phylogeography of Oryzomys couesi and Ototylo‐ mys phyllotis: historic and geographic implications for the Cen‐ tral America conformation Tania Anaid Gutiérrez‐García PhD Thesis, Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Torre II de Humanidades, Ciudad Universitaria, México DF, 04510, México; [email protected]

Abstract. Central America is an ideal region for comparative phylogeographic studies because of its intri‐ cate geologic and biogeographic history, diversity of habitats and dynamic climatic and tectonic history. The aim of this work was to assess the phylogeography of two rodents codistributed throughout Central America, in order to identify if they show concordant genetic and phylogeographic patterns. The synop‐ sis includes four parts: (1) an overview of the field of comparative phylogeography; (2) a detailed review that describes how genetic and geologic studies can be combined to elucidate general patterns of the biogeographic and evolutionary history of Central America; and a phylogeographic analysis of two spe‐ cies at both the (3) intraspecific and (4) comparative phylogeographic levels. The last incorporates spe‐ cific ecological features and evaluates their influence on the species’ genetic patterns. Results showed a concordant genetic structure influenced by geographic distance for both rodents, but dissimilar disper‐ sal patterns due to ecological features and life history. Keywords. climate, genetic diversity, geology, Middle America, Muridae

Introduction tinct phylogeographic patterns, suggesting that Over the past century, Central America (CA) has ecology and life history traits, among others, also been recognized as a geographic region with explain the genetic distribution observed (Sullivan highly complicated geology and climate dynamics, et al. 2000). in which processes like speciation, extinction and Oryzomys couesi and Ototylomys phyllotis diversification gave rise to a variety of multiscale are rodents that are codistributed in Central genetic and phylogeographic patterns. To under‐ America. O. couesi ranges from Colombia stand those patterns, biogeographers have incor‐ throughout CA to northern Mexico along the Pa‐ porated in their analyses methods developed for cific, the Gulf of Mexico and the Caribbean coasts, the field of intraspecific and comparative phy‐ while O. phyllotis occurs in a smaller area, from logeography (CP). Comparative phylogeographic Costa Rica to the Isthmus of Tehuantepec (Figure studies rely on the assumption that the most par‐ 1). These species have different habitat prefer‐ simonious explanation for concordant phy‐ ences and ecological characteristics (Lawlor 1982, logeographic patterns among different species is Reid 1997). Few studies about these species exist, that they arise because of a shared biogeographic their genetics having been used mainly to describe or evolutionary history (Bermingham and Martin the phylogenetic relationships of major rodent 1995, Avise 2000, Arbogast and Kenagy 2001). To groups (i.e., Steppan et al. 2004, Reeder et al. test this assumption, CP studies evaluate species 2006, Weksler 2006) and population genetics at that have a shared distribution; for example many local scales (for O. couesi only; i.e., Vega et al. species are codistributed along CA and, conse‐ 2007). Accordingly, the main objectives of this quently, likely have been affected by similar geo‐ work were to evaluate the intraspecific and com‐ logic and biogeographic processes that defined parative phylogeographic patterns of the two ro‐ much of their evolutionary history. As a result, CP dent species and assess if they have a concordant studies have found concordant phylogeographic phylogeographic response to their shared geologic patterns, but also cases where species show dis‐ and climatic history. The influence of their eco‐

Figure 1. Scheme of distribu‐ tion and phylogeographic bar‐ riers of Oryzomys couesi and Ototylomys phyllotis. The pale green, dashed blue lines and dashed square are used for O. couesi, while the intense green, solid red lines and solid square are used for O. phyl‐ lotis. The yellow regions show where are located the phy‐ logroups shared among spe‐ cies, the lines indicate the main barriers (climatic and/or geological) associated with the conformation of the major phylogroups and squares indi‐ cate the area of origin of each species according to this study.

logical characteristics on the patterns observed gence of the area as an archipelago until the was also assessed. emergence of the Isthmus of Panama and forma‐ tion of CA as a continuous landmass. It follows Materials and Methods with the account of the species exchange between Study System North/South America and CA as: a first migration during the Late Cretaceous‐Early Paleocene, a sec‐ The first two chapters of Gutiérrez‐García (2013) ond through a terrestrial corridor preceding the are published reviews, one that focuses on the formation of the Isthmus of Panama (IP), and the development of the field of comparative phy‐ third involving a major dispersion through the IP. logeography (CP) and the evolution of the meth‐ Finally, it illustrates how such events, together ods used for its analyses (Gutiérrez‐García and with the geologic history, caused similar genetic Vázquez‐Domínguez 2011) and the other that de‐ differentiation patterns and left a signature on the fines how genetic and geologic studies can be diversification of the taxa distributed along this combined to elucidate general patterns of the bio‐ region. geographic and evolutionary history of Central

America (CA) and of its biota (Gutiérrez‐García and Vázquez‐Domínguez 2013). Gutiérrez‐García Phylogeographic Analyses and Vázquez‐Domínguez (2011) describes the The third chapter of Gutiérrez‐García (2013) is the characteristics that shape a CP study, and summa‐ study of the geographic distribution and genetic rizes the field’s primary theoretical, methodologi‐ diversity of O. phyllotis based on 132 sequences of cal, and analytical requirements, frequent hy‐ a fragment of cytochrome b (Gutiérrez‐García and potheses tested, and current achievements and Vázquez‐Domínguez 2012). It includes a diverse limitations, including a variety of illustrative exam‐ array of phylogeographic tools and analyses to ples throughout. Gutiérrez‐García and Vázquez‐ describe the evolution of the species to its present Domínguez (2013) describes the geologic and tec‐ distribution, including the different diversification, tonic evolution of CA, from the gradual emer‐ dispersal and geologic patterns involved. frontiers of biogeography 5.4, 2013 — © 2013 the authors; journal compilation © 2013 The International Biogeography Society 239 comparative genetics of Central America rodents

Finally, the fourth chapter of Gutiérrez‐ gested for some O. phyllotis phylogroups. Multi‐ García (2013) describes the phylogeography of O. variate analysis indicated that genetic structure couesi and focuses mainly on the comparison be‐ between lineages is significantly associated with tween the phylogeographic patterns of both spe‐ the phylogeographic hypothesis for both species, cies. With this purpose, 201 sequences of a cyto‐ while structure at the level of populations within chrome b fragment of O. couesi were analyzed lineages is explained by the ecological (O. couesi) and the phylogeographic patterns determined in and morphological (O. phyllotis) hypotheses. Fi‐ much the same way as for O. phyllotis. Next, the nally, ecological variables are significantly associ‐ haplotypes from within the area of codistribution ated with structure at the level of individuals of the two species were grouped based on the within populations. Precipitation was the primary following criteria: (1) morphology, (2) geographic significant ecological variable for both species, and genetic distances, (3) phylogenetic groups, although altitude and temperature variables were i.e., clades obtained with maximum likelihood and also important for O. couesi. Bayesian phylogenetic estimators, and (4) consid‐ ering 19 environmental variables (BIOCLIM) and Discussion altitude values. These groups were analyzed with The comparative phylogeography of two different genetic and multivariate statistics in or‐ Neotropical rodents, O. couesi and O. phyllotis, der to test which of four hypotheses with overlapping distribution in Mexico and Cen‐ (morphological, phylogeographic, phylogenetic tral America, show that these species have shared and ecological) more significantly explain the ge‐ their geographic range at least for the past 3 Myr. netic structuring of the species (i.e., different line‐ A ‘mixed’ phylogeographic response can be de‐ ages). scribed, where both species have concordant pat‐ terns for two of the lineages or phylogroups iden‐ Results tified for each species: Central America and Yuca‐ Ototylomys phyllotis showed high to moderate tan peninsula. These lineages have a genetic and genetic diversity, with three major phy‐ phylogeographic structure influenced by major logeographic lineages whose distribution coin‐ geologic features and climatic events (mountains, cides with the main geological features that volcanic chains and diverse barriers like the Isth‐ shaped Middle America. The origin of the genus mus of Tehuantepec), together with the emer‐ was before 3.35 ± 0.21 million years ago (Myr), gence of the Isthmus of Panama that triggered the prior to the Great American Biotic Interchange Great American Biotic Interchange. The dispersal (GABI), and its initial occurrence was near the cen‐ and diversification of both rodents are tightly tre of its current distribution (Honduras/El Salva‐ linked to the geologic and climatic history of the dor, Fig. 1), from which it later spread (3.20 ± 0.19 region, with extremely high genetic diversity oc‐ Myr) following a series of GABI pulses (Gutiérrez‐ curring throughout the entire range, the highest García and Vázquez‐Domínguez 2012). Oryzomys of which was in the Yucatan peninsula, where the couesi has an origin in southern Central America phylogroups of both species experienced range (Fig. 1), also with high to moderate genetic diver‐ expansion. Also, at a smaller geographic and evo‐ sity values, and is divided into seven phy‐ lutionary scale, results showed evidence that ge‐ logeographic groups. Out of the total number of netic structuring of populations is associated with phylogroups, the two species coincide only in the the species’ ecological characteristics, identifying conformation of two, one located in Central some climatic and morphological variables signifi‐ America (Honduras, Guatemala, Nicaragua and cantly associated with their genetic structures. On Costa Rica) and one located along the Yucatan the other hand, discordant patterns also were ob‐ peninsula in southern Mexico. Additionally, both served: the origin and subsequent dispersal of the species show demographic signatures of popula‐ two species were not similar (Fig. 1), and their tion expansion, but potential bottlenecks are sug‐ ecological features and species‐specific life‐history

characteristics resulted in mixed responses to Gutiérrez‐García, T.A. & Vázquez‐Domínguez, E. (2011) Com‐ some vicariant events. A study like the present, parative phylogeography: designing studies while surviving the process. BioScience, 61, 857–868. which involved species with different ecological Gutiérrez‐García, T.A. & Vázquez‐Domínguez, E. (2012) Bio‐ requirements, origin and life history, codistributed geographically dynamic genetic structure bridging in a biogeographically complex area like Central two continents in the monotypic Central American rodent Ototylomys phyllotis. Biological Journal of the America, is ideal to test hypotheses about con‐ Linnean Society of London, 107, 593–610. certed and/or independent phylogeographic re‐ Gutiérrez‐García, T.A. & Vázquez‐Domínguez, E. (2013) Con‐ sponses. sensus between genes and stones in the bio‐ geographic and evolutionary history of Central Amer‐ ica. Quaternary Research, 79, 311–324. Acknowledgements Lawlor, T.E. (1982) Ototylomys phyllotis. Mammalian Species, 181, 1–3. I would like to give special thanks to my advisor Reeder, S.A., Carroll, D.S., Edwards, C.W., Kilpatrick, C.W. & Dr. Ella Vázquez‐Domínguez, who directed and Bradley, R.D. (2006) Neotomine‐peromyscine rodent advised this work with professionalism and enthu‐ systematics based on combined analyses of nuclear and mitochondrial DNA sequences. Molecular Phy‐ siasm. I also thank my PhD committee members, logenetics and Evolution, 40, 251–258. Dr. Daniel Piñero and Dr. Enrique Martínez‐Meyer, Reid, F.A. (1997) A field guide to the mammals of Central for their support and valuable contributions. The America and Southeast Mexico. Oxford University Press, USA. PhD scholarship and financial support were pro‐ Steppan, S.J., Adkins, R.M. & Anderson, J. (2004) Phylogeny vided by the National Council of Science and Tech‐ and divergence‐date estimate of rapid radiations in nology (CONACyT) and the National Autonomous muroid rodents based on multiple nuclear genes. University of México (UNAM). This work was fi‐ Systematic Biology, 53, 533–553. Sullivan, J., Markert, J.A., & Kilpatrick, W. (1997) Phylogeogra‐ nanced by the following projects: PAPIIT IN215205 phy and molecular systematics of the Peromyscus ‐2, IX238004, IN21907 and CONACyT 101861. aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Systematic Biology, 46, 426–440. References Vega, R., Vázquez‐Domínguez, E., Mejía‐Puente, A. & Cuarón, Avise, J.C. (2000) Phylogeography: the history and formation A.D. (2007) Unexpected high levels of genetic variabil‐ of species. Harvard University Press, USA. ity and the population structure of an island endemic Arbogast, B.S. & Kenagy, G.J. (2001) Comparative phy‐ rodent (Oryzomys couesi cozumelae). Biological Con‐ logeography as an integrative approach to historical servation, 137, 210–222. biogeography. Journal of Biogeography, 28, 819–825. Weksler, M. (2006) Phylogenetic relationships of Oryzomine Bermingham, E. & Martin, A.P. (1998) Comparative mtDNA rodents (Muroidea: Sigmodontinae): separate and es of morphological and molecular phylogeography of Neotropical freshwater fishes: combined analys data. Bulletin of the American Museum of Natural testing shared history to infer the evolutionary land‐ scape of lower Central America. Molecular Ecology, 7, History, 296, 1–48. 499–517. Gutiérrez‐García, T.A. (2013) Filogeografía comparada de Edited by Carolina Tovar and Jessica Blois Oryzomys couesi y Ototylomys phyllotis; implicaciones históricas y geográficas en la conformación de México y Centro América. Tesis Doctoral, Universidad Nacio‐ nal Autónoma de México, Instituto de Ecología, 143 pp.