Skip to main content
SpringerLink
Log in

The Role of Geographical and Ecological Factors on Population Divergence of the Neotropical otter Lontra longicaudis (Carnivora, Mustelidae)

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The geographic distribution of the populations of a species are influenced by the spatial structure of the ecosystems, the environmental factors and the presence of geographic barriers. The Neotropical otter, Lontra longicaudis, is widely distributed throughout the Americas, where a wide range of environmental conditions and geographical features could promote genetic and morphological variation on the three currently recognized subspecies. In this study, we combined phylogeographic, morphometric and environmental niche modelling analyses to examine whether: (1) genetic variation is associated with the presence of barriers to gene flow and/or hydrography; (2) genetic and morphologic variation are associated with environmental variation; and (3) the observed variation in L. longicaudis populations corresponds to the previously defined subspecies. We found strong phylogeographic structure between the northern (L. l. annectens) and the two-southern subspecies (L. l. longicaudis and L. l. enudris), and although shallower, we also detected genetic differentiation between the two South American subspecies. Such genetic differentiation corresponds to the hydrography and to the geographical barriers characteristic of the distributional area of the species. We found a correlation between the shape of the skull and mandible with the environmental variation through the distribution of the species, and we rejected the hypothesis of niche equivalency and similarity between the three identified genetic lineages, suggesting adaptations to different environmental conditions. Our results support that the variation in environmental conditions, in concert with geographical barriers to gene flow and hydrography, have led to population divergence of L. longicaudis along the Neotropics. These results have important taxonomic implications for the species and its conservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alfaro, M. E., & Huelsenbeck, J. P. (2006). Comparative performance of Bayesian and AIC-Based measures of phylogenetic model uncertainty. Systematic Biology, 55, 189–196.

    Article  Google Scholar 

  • Alvarado-Serrano, D. F., & Knowles, L. (2014). Ecological niche models in phylogeography studies: Applications, advances and precautions. Molecular Ecology, 14, 233–248.

    Article  Google Scholar 

  • Anderson, R., Lew, D., & Peterson, A. (2003). Evaluating predictive models of species’ distributions: Criteria for selecting optimal models. Ecological Modelling, 162, 211–232.

    Article  Google Scholar 

  • Antonelli, A., Quijada-Masareñas, A., Crawford, A. J., Bates, J. M., Velazco, P. M., et al. (2010). Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In C. Hoorn & F. Wesselingh (Eds.), Amazonia landscape and species evolution: A look in to the past. (pp. 386–404) Chichester: Wiley-Blackwell.

    Google Scholar 

  • Argollo, J. (2006). El río Parapentí y los Bañados del Izozoc, Bolivia. Revista UnG Geociéncias, 5, 38–44.

    Google Scholar 

  • Avise, J. C. (2000). Phylogeography: the history and formation of species. Cambridge: Harvard.

    Google Scholar 

  • Ayres, J. M. C., & Clutton-Brock, T. H. (1992). River boundaries and species range size in Amazonian primates. The American Naturalist, 140, 531–537.

    Article  CAS  PubMed  Google Scholar 

  • Baker, R. J., & Bradley, R. D. (2006). Speciation in mammals and the genetic species concept. Journal of Mammalogy, 87, 643–666.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bandelt, H., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Banguera-Hinestroza, E., Cardenas, H., Ruiz-García, M., Marmontel, M., Gaitan, E., et al. (2002). Molecular Identification of evolutionarily significant units in the Amazon river dolphin Inia sp. (Cetacea: Iniidae). Journal of Heredity, 93, 312–322.

    Article  CAS  PubMed  Google Scholar 

  • Barbanti Duarte, J. M., Gonzalez, S., & Maldonado, J. E. (2008). The surprising evolutionary history of South American deer. Molecular Phylogenetics and Evolution, 49, 17–22.

    Article  CAS  Google Scholar 

  • Barve, N. (2008). Tool for partial-ROC, ver 1.0. Lawrence, KS: Biodiversity Institute.

  • Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S. P., et al. (2011). The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling, 222, 1810–1819.

    Article  Google Scholar 

  • Beheregaray, B. L., Cooke, M. G., Chao, L. N., & Landguth, L. E. (2015). Ecological speciation in the tropics: Insights from comparative genetic studies in Amazonia. Frontiers in Genetics. doi: 10.3389/fgene.2014.00477.

    PubMed  PubMed Central  Google Scholar 

  • Bermingham, E., & Martin, A. P. (1998). Comparative mtDNA phylogeography of neotropical freshwater fishes: Testing shared history to infer the evolutionary landscape of lower Central America. Molecular Ecology, 4, 499–517.

    Article  Google Scholar 

  • Broennimann, O., Fitzpatrick, M. C., Pearman, P. B., Petitpierre, B., Pellissier, L., et al. (2012). Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography, 21, 481–497.

    Article  Google Scholar 

  • Bonaccorso, E., Koch, I., & Peterson, A. T. (2006). Pleistocene fragmentation of Amazon species’ ranges. Diversity and Distributions, 12, 157–164.

    Article  Google Scholar 

  • Bush, M. B., Silman, M. R., & Urrego, D. H. (2004). 48,000 years of climate and forest change in a biodiversity hot spot. Science, 303, 827–829.

    Article  CAS  PubMed  Google Scholar 

  • Cabrera, A. (1957). Catálogo de los mamíferos de América del Sur. I (Metatheria-Unguiculata-Carnivora). Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, 4, 1–307.

    Google Scholar 

  • Cardini, A., Jansson, A. U., & Elton, S. (2007). A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys. Journal of Biogeography, 34, 1663–1678.

    Article  Google Scholar 

  • Centrón, D., Ramirez, B., Fasola, L., Macdonald, D. W., Chehebar, C., et al. (2008). Diversity of mtDNA in southern river Otter (Lontra provocax) from Argentinean Patagonia. Journal Hered, 99, 198–201.

    Article  CAS  Google Scholar 

  • Chapman, M. R., & Chepstow-Lusty, A. J. (1997). Late Pliocene climatic change and the global extinction of the discoasters: An independent assessment using oxygen isotope records. Palaeogeography, Palaeoclimatology, Palaeoecology, 134, 109–125.

    Article  Google Scholar 

  • Chaput-Bardy, A., Fleurant, C., Lemaire, C., & Secondi, J. (2009). Modeling the effect of in-stream and overland dispersal on gene flow in river networks. Ecological Modelling, 220, 3589–3598.

    Article  Google Scholar 

  • Claude, J., Pritchard, P., Tong, H., Paradis, E., & Aufray, J. (2004). Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment. Systematic Biology, 53, 933–948.

    Article  PubMed  Google Scholar 

  • Cooke, G. M., Chao, N. L., & Beheregaray, L. B. (2012). Divergent natural selection with gene flow along major environmental gradients in Amazonia: insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus. Molecular Ecology, 21, 2410–2427.

    Article  PubMed  Google Scholar 

  • Cooke, G. M., Chao, N. L., & Beheregaray, L. B. (2014). River scape genetics identifies replicated ecological divergence across an Amazonian ecotone. Evolution. doi:10.1111/evo.12410.

    PubMed  Google Scholar 

  • Cortés-Oritz, L., Bermonham, E., Rico, C., Rodríguez-Luna, E., Sampaio, I., & Ruíz-García, M. (2003). Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26, 64–81.

    Article  Google Scholar 

  • Costello, A. B., Down, T. E., Pollard, S. M., Pacas, J. C., & Taylor, E. B. (2002). The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus. (Pisces:Salmonidae). Evolution, 57, 328–344.

    Article  Google Scholar 

  • Cotler, H., & Pineda, R. (2008). Manejo integral de cuencas en México ¿hacia dónde vamos? Archivo Histórico del Agua, 39, 16–21. https://biblat.unam.mx/es/revista/boletin-del-archivo-historico-del-agua/articulo/manejo-integral-de-cuencas-en-mexico-hacia-donde-vamos

  • Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates Press.

    Google Scholar 

  • Crait, J. R., Prange, H. D., Marshall, N. A., Harlow, H. J., Cotton, C. J., & Ben-David, M. (2012). High-altitude diving in otters: Coping with combined hypoxic stresses. Journal Experimental Biology, 215, 256–263.

    Article  CAS  Google Scholar 

  • Crandall, K. A., & Templeton, A. R. (1993). Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics, 134, 959–969.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuevas, M. L., Garrido, A., & Sotelo, E. I. (2011). Regionalización de las cuencas hidrogáficas de México. In H Cotler (Ed.), Las cuencas hidrográficas de México: Diagnostico y priorización. (p. 232). Puebla: Instituto Nacional de Ecología. ISBN 978-607-7655-07-7.

    Google Scholar 

  • De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886.

    Article  PubMed  Google Scholar 

  • de Thoisy, B., Ruiz-Garcia, M., Castellanos-Mora, L., & Laverne, A. (2013). How are the Amazon and Orinoco rivers related? Preliminary results on the comparative history, structure and dynamics of Pteronura brasiliensis, from Western Amazonia. In M. Ruiz-Garcia & J. M. Shostell (Eds.), Molecular population genetics, evolutionary biology and biological conservation of neotropical carnivores (pp. 85–96). Hauppauge: Nova Science Publishers.

    Google Scholar 

  • Dellicour, S., & Mardulyn, P. (2014). SPADS. Ver. 1.0: A toolbox to perform spatial analyses on DNA sequence data sets. Molecular Ecology Resources, 14, 647–651.

    Article  PubMed  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.8. Molecular Biology and Evolution, 29, 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duque-Caro, H. (1990). Estratigrafía, paleoceanografía y paleobiogeografía de la cuenca del Atrato y la evolución del Istmo de Panamá. Boletin Geológico, 31, 3–6.

    Google Scholar 

  • Eberhard, J. E., & Bermingham, E. (2005). Phylogeny and biogeography of the Amazona ochrocephala (Aves: Psittacidae) complex. The Auk, 121, 318–332.

    Article  Google Scholar 

  • Eizirik, E., Kim, J., Menotti-Raymond, M., Grawshaw, P. G. Jr., O´Brien, S. J., & Johnson, W. E. (2001). Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Molecular Ecology, 10, 67–79.

    Article  Google Scholar 

  • Elith, J., Graham, C. H., Anderson, R. P., Dudík, M., Ferrier, S., Guisan, A., et al. (2006). Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 29, 129–151.

    Article  Google Scholar 

  • Elith, J., Phillips, S. J., Hastie, T., Dudík, M., Chee, Y. E., et al. (2011). A statistical explanation of maxent for ecologists. Diversity and Distributions, 17, 43–57.

    Article  Google Scholar 

  • Emmons, L. H., & Feer, F. (1997). Neotropical rainforest mammals: A field guide. Chicago: The University of Chicago Press.

    Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin v3.1. An integrated software package for population genetics data analysis. Retrieved from Feb 23, 2005 http://cmpg.unibe.ch/software/arlequin3.

  • Garcia, D. M., Marmontel, M., Rosas, F. W., & Santos, F. R. (2007). Conservation genetics of the giant otter (Pteroura brasiliensis) (Zimmerman, 1780) (Carnivora: Mustelidae). Brazilian Journal of Biology, 67, 631–637.

    Google Scholar 

  • Gillman, L. N., Keeling, D. J., Ross, H. A., & Wright, S. D. (2009). Latitude, elevation and the tempo of molecular evolution in mammals. Proceedings of the Royal Society—Biological Sciences, 276, 3353–3359.

    Article  PubMed  PubMed Central  Google Scholar 

  • Graham, C. H., Silva, N., & Velásquez-Tibatá, J. (2010). Evaluating the potential causes of range limits of birds of the Colombian Andes. Journal of Biogeography, 37, 1863–1875.

    Google Scholar 

  • Guerrero, J., Gallo-Reynoso, J. P., & Biek, R. (2015). Mitochondrial DNA diversity, genetic structure and demographic history of the Neotropical otter (Lontra longicaudis) in Mexico. Journal of Mammalogy. doi:10.1093/jmammal/gyv124.

    Google Scholar 

  • Haffer, J. (1997). Alternative models of vertebrate speciation in Amazonia: an overview. Biodiversity and Conservation, 6, 451–476.

    Article  Google Scholar 

  • Haffer, J. (2008). Hypothesis to explain the origin of the species in Amazonia. Brazilian Journal of Biology, 68, 917–947.

    Article  CAS  Google Scholar 

  • Hansen, H., Ben-David, M., & McDonald, D. B. (2008). Effects of genotyping protocols on success and errors in identifying individual river otter (Lontra canadensis) from their feces. Molecular Ecology, 8, 282–289.

    Article  CAS  Google Scholar 

  • Harris, C. J. (1968). Otters: A study of the recent Lutrinae. London: Weinfield and Nicholson.

    Google Scholar 

  • Hernández-Romero, P. C., Guerrero, J. A., & Valdespino, C. (2015). Morphological variability of the cranium of Lontra longicaudis (Carnivora: Mustelidae): a morphometric and geographic analysis. Zoological Studies. doi: 10.1186/s40555-015-0127-6.

    Google Scholar 

  • Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London, 359, 183–195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hey, J. (2006). Recent advances in assessing gene flow between diverging populations and species. Current Opinion in Genetics and Development, 16, 592–596.

    Article  CAS  PubMed  Google Scholar 

  • Hey, J., & Nielsen, R. (2007). Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceeding of the National Academy of Sciences, 104, 2785–2790.

    Article  CAS  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.

    Article  Google Scholar 

  • Hoorn, C., Guerrero, J., Sarmiento, G. A., & Lorente, M. A. (1995). Andean tectonics as a cause for changing drainage patterns in Miocene northern South America. Geology, 23, 237–240.

    Article  Google Scholar 

  • Hrbek, T., da Silva, V., M, F., Dutra, N., Gravena, W., Martin, A. R., & Farias, I. P. (2014). A new species of river dolphin from Brazil or: How little do we know our biodiversity. PLoS ONE, 9, e83623. doi:10.1371/journal.pone.0083623.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hubert, H., & Renno, J. F. (2006). Historical biogeography of South American freshwater fishes. Journal of Biogeography, 33, 1414–1436.

    Article  Google Scholar 

  • Huelsenbeck, J. L., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, J. M., Schmidt, D. J., & Finn, D. S. (2009). Genes in streams: Using DNA to understand the movement of freshwater fauna and their riverine habitat. BioScience, 59, 573–583.

    Article  Google Scholar 

  • Jensen, J. L., Bohonak, A. J., & Kelley, S. T. (2005). Isolation by distance Ver 3.23. [Computer software and manual], Retrieved from March 11, 2005 http://ibdws.sdsu.edu/.

  • Johnson, W. E., Slattery, J. P., Eizirik, E., Kim, J.-H., & Raymond Menotti, M., et al. (1999). Disparate phylogeographic patterns of molecular genetic variation in four closely related South American small cat species. Molecular Ecology, 8, 79–94.

    Article  Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Kimura, M. (1981). Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences, 78, 454–458.

    Article  CAS  Google Scholar 

  • Koepfli, K. P., Deere, K., Slater, G. J., Begg, C., Begg, K., et al. (2008). Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biology, 6, 10.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koepfli, K. P., & Wayne, R. K. (1998). Phylogenetics relationships of otters (Carnivora: Mustelidae) based on mitochondrial cytochrome b sequences. Journal of Zoology, 24, 401–416.

    Article  Google Scholar 

  • Kruuk, H. (2006). Otter’s ecology, behavior and conservation. London: Oxford.

    Google Scholar 

  • Kuhner, M. K., & Smith, L. P. (2007). Comparing likelihood and Bayesian coalescent estimation of population parameters. Genetics, 175, 155–165.

    Article  PubMed  PubMed Central  Google Scholar 

  • Langerhans, B. R., Layman, C. A., Langerhans, A. K., & Dewitt, T. J. (2003). Habitat-associated morphological divergence in two Neotropical fish species. Biological Journal of the Linnean Society, 80, 689–698.

    Article  Google Scholar 

  • Larivière, S. (1999). Lontra longicaudis, Olfers 1818. Mammalian Species, 609, 1–5.

    Google Scholar 

  • Larsen, P. A., Hoofer, S. R., Bozeman, M. C., Pedersen, S. C., Genoways, H., et al. (2007). Phylogenetics and phylogeography of the Artibeus jamaicensis complex based on cytochrome-b DNA sequences. Journal of Mammalogy, 88, 712–727.

    Article  Google Scholar 

  • Laurito, C., & Valerio, A. (2012). Paleobiogeografía del arribo de mamíferos suramericanos al sur de américa central de previo al gran intercambio biótico americano: un vistazo al GABI en América Central. Revista Geológica de América Central, 46, 123–144.

    Google Scholar 

  • Lobo, J. M., Jiménez-Valverde, A., & Real, R. (2008). AUC: A misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography, 17, 145–151.

    Article  Google Scholar 

  • Lundberg, J. G., Marshall, L. G., Guerrero, J., Horton, B., Malabarba, M. C. S. L., et al. (1998). The stage for Neotropical fish diversification: a history of tropical South American rivers. In L. R. Malabarba, R. E. Reis, R. P. Vari, Z.M.S. Lucena & C.A.S. Lucena (Eds.), Phylogeny and classification of neotropical fishes. Part 1—fossils and geological evidence (pp. 14–48). Porto Alegre: Edipucrs.

    Google Scholar 

  • Manni, F., Guérard, E., & Heyer, E. (2004). Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Human Biology, 76, 173–190.

    Article  PubMed  Google Scholar 

  • Marmi, J., López-Giráldez, J. F., & Domingo-Roura, X. (2004). Phylogeny, evolutionary history and taxonomy of Mustelidae based of sequences of the cytrochrome b gene and a complex repetitive flanking region. Zoological Scripta, 33, 481–499.

    Article  Google Scholar 

  • Meade, R. H., & Koehnken, L. (1991). Distribution of the river dolphin, tonina Inia geoffrensis, in the Orinoco river basin of Venezuela and Colombia. Interciencia, 16, 300–312.

    Google Scholar 

  • Mongomery, D. R., Grant, G. E., & Sullivan, K. (1995). Watershed analysis as a framework for implementing ecosystem management. Water Resources Bulletin, 3, 369–386.

    Article  Google Scholar 

  • Montoya-Burgos, J. I. (2003). Historical biogeography of the catfish genus Hypostomus (Siluriformes: Loricariidae), with implications on the diversification of Neotropical ichthyofauna. Molecular Ecology, 12, 1855–1867.

    Article  CAS  PubMed  Google Scholar 

  • Morales-Jimenez, A. L., Disotell, T., & Di Fiore, A. (2015). Revisiting the phylogenetic relationships, biogeography, and taxonomy of spider monkeys (genus Ateles) in light of new molecular data. Molecular Phylogenetics and Evolution, 82, 467–483.

    Article  PubMed  Google Scholar 

  • Moritz, C. (1994). Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology and Evolution, 9, 373–375.

    Article  CAS  PubMed  Google Scholar 

  • Moritz, C., Patton, J. L., Schneider, C. J., & Smith, T. B. (2000). Diversification of rainforest faunas: An integrated molecular approach. Annual Review of Ecology and Systematics, 31, 533–563.

    Article  Google Scholar 

  • Noruésis, M. J. (2011). IBM SPSS statistics Ver. 19. [Computer software and manual]. London: Pearson Education.

    Google Scholar 

  • Padial, J. M., Miralles, A., De la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in zoology, 7, 16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Patton, J. L., & Da Silva, M. N. F. (1998). Rivers, refuges and ridges: the geography of speciation of Amazonian mammals. In S. Berlocher & D. Howard (Eds.), Endless forms: Species and speciation (pp. 202–216). London: Oxford.

    Google Scholar 

  • Perdices, A., Doadrio, I., Economidis, P. S., Bohlen, J., & Banarescu, P. (2003). Pleistocene effects on the European freshwater fish fauna: double origin of the cobitid genus Sabanejewia in the Danube basin (Osteichthyes: Cobitidae). Molecular Phylogenetic and Evolution, 26, 289–299.

    Article  CAS  Google Scholar 

  • Peterson, A. T., Papeş, M., & Soberón, J. (2008). Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling, 213, 63–72.

    Article  Google Scholar 

  • Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259.

    Article  Google Scholar 

  • Pickles, R. S. A., Grommbridge, J. J., Zambrana, R. V. D., Van Damme, P., Gottelli, D., et al. (2011). Evolutionary history and identification of conservation units in the giant otter, Pteronura brasiliensis. Molecular Phylogenetics and Evolution, 61, 616–627.

    Article  CAS  PubMed  Google Scholar 

  • Pilot, M., Jedrzejewski, W., Branicki, W., Sidrovich, V. E., Jedrzejewska, B., et al. (2006). Ecological factors influence population genetic structure of European grey wolf. Molecular Ecology, 15, 4533–4553.

    Article  CAS  PubMed  Google Scholar 

  • Pohle, H. (1920). Die Unterfamilie der Lutrinae. Eine systematisch-tiergeographische Studie an dem Material der Berliner Messen. Archiv für Naturgeschichte, 1920, 1–247.

    Google Scholar 

  • Pons, O., & Petit, R. J. (1996). Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics, 144, 1237–1245.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Posada, D., & Crandall, K. A. (1998). MODELTEST: Testing the model of DNA substitution. Bioinformatics (Oxford, England), 14, 817–818.

    Article  CAS  Google Scholar 

  • Prance, G. T. (1982). Biological diversification in the tropics. New York: Columbia University Press.

    Google Scholar 

  • Pyron, R. A., & Burbrink, T. F. (2010). Hard and soft allopatry: physically and ecologically mediate models of geographic speciation. Journal of Biogeography, 37, 2005–2015.

    Google Scholar 

  • Rambaut, A. (2014). FigTree Ver. 1.4.2. [Computer software and manual]. Retrieved from May 11, 2015 http://tree.bio.ed.ac.uk/software/figtree/.

  • Rambaut, A., & Drummond, A. J. (2007). Tracer analysis tool version 1.4. [Computer software and manual]. Oxford: University of Oxford.

    Google Scholar 

  • Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). Tracer v1.6. Available from http://tree.bio.ed.ac.uk/software/tracer/.

  • Reed-Smith, J. (2012). North american river otter husbandry notebook. Michigan: Grand Rapids Press.

    Google Scholar 

  • Rheingantz, M. L., Saraiva De Menezes, J. F., & Thoisy, B. (2014). Defining Neotropical otter Lontra longicaudis distribution, conservation priorities, and ecological frontiers. Tropical Conservation Science, 7, 214–229.

    Article  Google Scholar 

  • Rheingantz, M. L., & Trinca, C. S. (2015). Lontra longicaudis. London: The IUCN Red List of Threatened Species.

    Google Scholar 

  • Rheingantz, M. L., Santiago-Plata, V., & Trinca, C. S. (2017). The neotropical otter Lontra longicaudis: A comprehensive update on the current knowledge and conservation status of this semiaquatic carnivore. Mammal Review. doi:10.1111/mam.12098.

    Google Scholar 

  • Ricklefs, R. E., & Miles, D. B. (1994). Ecological and evolutionary inferences from morphology: An ecological perspective. In P. C. Wainwright & S. M. Reilly (Eds.), Ecological morphology: Integrative organismal biology (pp. 13–41). Chicago: The University of Chicago Press.

    Google Scholar 

  • Rogers, A. R., & Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Ecology and Evolution, 9, 552–569.

    CAS  Google Scholar 

  • Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49, 740–753.

    Article  CAS  PubMed  Google Scholar 

  • Rüber, L., & Adams, D. C. (2001). Evolutionary convergence of body shafe and trophic morphology in cichlids fron the Lake Tanganyika. Journal of Evolutionary Biology, 14, 325–332.

    Article  Google Scholar 

  • Ruiz-García, M., Vásquez, C., Pinedo-Castro, M., Sandoval, S., Castellanos, A., et al. (2012). Phylogeography of the Mountain Tapir (Tapirus pinchaque) and the Central American Tapir (Tapirus bairdii) and the Origins of the Three Latin-American Tapirs by Means of mtCyt-B Sequences, In K. Anamthawat-Jónsson (Ed.), Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems. (pp. 83–116). Rijeka: In Tech.

    Google Scholar 

  • Schneider, S., & Excoffier, L. (1999). Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetic, 152, 1079–1089.

    CAS  Google Scholar 

  • Schoener, T. W. (1968). Anolis lizards of Bimini: Resource partitioning in a complex fauna. Ecology, 49, 704–726.

    Article  Google Scholar 

  • Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64, 295–315.

    Article  PubMed  Google Scholar 

  • Soberón, J., & Peterson, A. T. (2005). Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Information, 2, 1–10.

    Google Scholar 

  • Soibelzon, L., & Prevosti, F. J. (2007). Los carnívoros (Carnivora, Mammalia) terrestres del Cuaternario de América del Sur. In G. X. Pons & D. Vicens (Eds.), Geomorfología Litoral i Quaternari. Homenatge a Joan Cuerda Barceló (pp. 49–68). Palma de Mallorca: Mon. Soc. Hist. Nat. Balears Press.

    Google Scholar 

  • Soto-Centeno, J. A., Barrow, L. N., Allen, J. M., & Reed, D. L. (2013). Reevaluation of a classic phylogeographic barrier: New techniques reveal the influence of microgeographic climate variation on population divergence. Ecology and Evolution, 3, 1603–1613.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamataks, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mix models. Bioinformatics, 22, 2688–2690.

    Article  CAS  Google Scholar 

  • Stohlgren, T. J., Jarnevich, C. S., Esaias, W. E., & Morisette, J. T. (2001). Bounding species distribution models. Current Zoology, 57, 642–647.

    Article  Google Scholar 

  • Swinkels, L. H., Van de Ven, M. W. P. M., Stassen, M. J. M., Van der Velde, G., Lenders, H. J. R., et al. (2012). Suspended sediment causes acute fish mortality in the Pilcomayo River (Bolivia). Hydrological Processes. doi:10.1002/hyp.9522.

    Google Scholar 

  • Sztencel-Jabłonka, A., Jones, G., & Bogdanowicz, W. (2009). Skull morphology of two cryptic bat species: Pipistrellus pipistrellus and P. pygmaeus a 3D geometric morphometrics approach with landmark reconstruction. Acta Chiropterologica, 11, 113–126.

    Article  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis. Ver. 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.

    CAS  PubMed  Google Scholar 

  • Tchaicka, L., Eizirik, E., De Oliveira, T. G., Cándido, J. F. Jr., & Freitas, T. R. O. (2007). Phylogeography and population history of the crab-eating fox (Cerdocyonthous). Molecular Ecology, 16, 819–838.

    Article  CAS  PubMed  Google Scholar 

  • Toivonen, T., Maki, S., & Kalliola, R. (2007). The riverscape of Amazonia a quantitative approach to the fluvial biogeography of the region. Journal of Biogeography, 34, 1374–1387.

    Article  Google Scholar 

  • Trigo, T. C., Freitas, T. R. O., Kunzler, G., Cardoso, L., Silva, J. C. R., et al. (2008). Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyiand and L. tigrinusin southern Brazil. Molecular Ecology, 17, 4317–4333.

    Article  CAS  PubMed  Google Scholar 

  • Trinca, C. S., Fernandes-Jaeger, C., & Eizirik, E. (2013). Molecular ecology of the Neotropical otter (Lontra longicaudis): Non-invasive sampling yields insights into local population dynamics. Biological Journal of the Linnean Society, 109, 932–948.

    Article  Google Scholar 

  • Trinca, C. S., Thoisy, B., Rosas, F., Waldemarin, H. F., Koepfli, K. P., et al. (2012). Phylogeography and demographic history of the Neotropical otter (Lontra longicaudis). Journal of Heredity, 103, 479–492.

    Article  PubMed  Google Scholar 

  • Trinca, C. S., Wlademarin, H. F., & Eizirik, E. (2007). Genetic diversity of Neotropical otter (Lontra longicaudis Olfers, 1818) in Southern and Southeastern Brazil. Brazil Journal Biology, 67, 813–818.

    Article  CAS  Google Scholar 

  • Turchetto-Zolet, A. C., Pinheiro, F., Salgueiro, F., & Palma-Silva, C. (2012). Phylogeographical patterns shed light on evolutionary process in South America. Molecular Ecology, 22, 1193–1213.

    Article  PubMed  Google Scholar 

  • USGS. (2015). Hydro 1 k. U.S.G. Survey (Ed.). https://lta.cr.usgs.gov/HYDRO1K.

  • Van der Hammen, T. (1992). Historia, Ecología y Vegetación de Bogotá, Colombia. Bogotá: Corporación colombiana para la Amazonía-Araracuara Press.

    Google Scholar 

  • van Zyll de Jong, C. G. (1972). A systematic review of the Nearctic and Neotropical river otters (Genus Lutra, Mustelidae, Carnivora). Royal Ontario Museum Life Sciences Contributions, 80, 112.

    Google Scholar 

  • Venegas-Anaya, M., Grawford, A. J., Escobedo, G. A. H., Sanjur, O. I., Densmore, L. D., et al. (2008). Mitochondrial DNA phylogeography of Caiman crocodilus in Mesoamerica and South America. Journal of Experimental Zoology, 309A, 614–627.

    Article  CAS  Google Scholar 

  • Vianna, J. A., Ayerdi, P., Medina-Vogel, G., Mangel, J. C., Zeballos, H., et al. (2010). Phylogeography of the marine otter (Lontra felina): Historical and contemporary factors determining its distribution. Journal of Heredity, 101(6), 676–689. doi:10.1093/jhered/esq088.

    Article  CAS  PubMed  Google Scholar 

  • Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution, 62, 2868–2883.

    Article  PubMed  Google Scholar 

  • Warren, D. L., Glor, R. E., & Turelli, M. (2010). ENMTools: A toolbox for comparative studies of environmental niche models. Ecography, 33, 607–611.

    Article  Google Scholar 

  • Webb, D. S. (1991). Ecography and the Great American Interchange. Paleobiology, 17(3), 266–280.

    Article  Google Scholar 

  • Weir, J. T., & Schluter, D. (2007). The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science, 315, 1574–1576.

    Article  CAS  PubMed  Google Scholar 

  • Whitemore, T. C., & Prance, G. T. (1987). Biogeography and Quaternary history in tropical America. Oxford: Oxford University Press.

    Google Scholar 

  • Wiens, J. J., & Graham, C. H. (2005). Niche conservatism: Integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519–539.

    Article  Google Scholar 

  • Willis, S. C., Nunes, M., Montaña, C. G., Farias, I. P., Prtís, G., et al. (2010). The Casiquiare River affects as a corridor between the Amazonas and Orinoco river basins: Biogeographic analysis of the generus Cichla. Molecular Ecology, 19, 1010–1030.

    Article  Google Scholar 

  • Wisely, S. M., Maldonado, J. E., & Fleischer, R. C. (2004). A tech-nique for sampling ancient DNA that minimizes damage to museum specimens. Conservation Genetics, 5, 105–107.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a Seed Fund Grant from the State University of New York (SUNY) to Carolina Valdespino and by the River Otter Grant 2013 from The River Otter Alliance (ROA) to Pablo C. Hernández-Romero. PCHR and DAP-T were supported by a Doctoral scholarship (323848 and 297538, respectively) from the Consejo Nacional de Ciencia y Tecnología (CONACyT, Mexico). We are grateful to the Acuario de Veracruz, A.C. and to the Zológico Benito Juárez in Morelia for sample donation. We thank Denisse Maldonado and Cristina Bárcenas for laboratory assistance and María Camila Latorre Cárdenas, Adriana Sandoval Comte, Policarpo Ronzón and Antonio Vázquez for field work assistance. José A. Guerrero, Ella Vázquez and Alejandro Espinosa de los Monteros provided valuable comments on earlier versions of this work.

Author information

Authors and Affiliations

  1. Red de Biología y Conservación de Vertebrados, Instituto de Ecología A.C., Carretera antigua a Coatepec 351, 91070, Xalapa, VER, Mexico

    Pablo C. Hernández-Romero & Carolina Valdespino

  2. Red de Biología Evolutiva, Instituto de Ecología A.C., Carretera antigua a Coatepec 351, 91070, Xalapa, VER, Mexico

    Carla Gutiérrez-Rodríguez & David A. Prieto-Torres

  3. Eje BioCiencias, Centro de Modelado Científico (CMC), Facultad Experimental de Ciencias, Universidad del Zulia, Av. Universidad calle No 65, Maracaibo, 4004, Estado Zulia, Venezuela

    David A. Prieto-Torres

Authors
  1. Pablo C. Hernández-Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carla Gutiérrez-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolina Valdespino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David A. Prieto-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo C. Hernández-Romero.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 6357 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Romero, P.C., Gutiérrez-Rodríguez, C., Valdespino, C. et al. The Role of Geographical and Ecological Factors on Population Divergence of the Neotropical otter Lontra longicaudis (Carnivora, Mustelidae). Evol Biol 45, 37–55 (2018). https://doi.org/10.1007/s11692-017-9428-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-017-9428-5

Keywords

Search

Navigation