Insights into the evolutionary and demographic history of the extant endemic rodents of the Galápagos Islands

Autores/as

  • Susette Castañeda-Rico Smithsonian Institution / George Mason University
  • Sarah A. Johnson George Mason University. Commission on Environmental Quality (TCEQ).
  • Scott A. Clement Angelo State University
  • Robert C. Dowler Angelo State University
  • Jesús E. Maldonado Center for Conservation Genomics, Smithsonian Conservation Biology Institute.
  • Cody W. Edwards George Mason University. Smithsonian-Mason School of Conservation.

Palabras clave:

Aegialomys, colonization, diversification, Nesoryzomys, populations, speciation.

Resumen

Evolutionary radiations stemming from colonization of archipelagos provide valuable insights into mechanisms and modes of speciation. For this reason, the fauna inhabiting the Galápagos Islands has been the focus of numerous emblematic ecological and evolutionary studies. However, studies focused on rodents have been scarce. Rice rats radiated in situ into at least seven endemic species: Aegialomys galapagoensis, Nesoryzomys narboroughi, N. swarthi, N. fernandinae, N. indefessus, N. darwini and Megaoryzomys curioi. Only the first four species remain extant on the archipelago. These species are considered vulnerable, mainly due to human activities and invasive species. Despite their interesting evolutionary history, questions surrounding phylogenetic relationships, colonization events, genetic diversity and demography of populations remain unresolved. We used the D-loop region of mtDNA to infer phylogenetic relationships, colonization events, date divergences, and conduct population genetic analyses of the four extant endemic species inhabiting the Galápagos Islands. We found that all species were monophyletic. A. galapagoensis is sister to A. xanthaeolus from the continent, and both of them are the sister clade of the genus Nesoryzomys. Our results also showed that there were two colonization events to the islands. The first event was the arrival of the ancestor of Nesoryzomys during the Pliocene, when divergences between genera occurred. The second was Aegialomys during middle Pleistocene, when species diversification began. Populations on each island show high genetic diversity and most show signals of recent expansion. However, future studies are needed to accurately assess the conservation status of these populations. We suggest ongoing monitoring of these vulnerable endemic species, including ecological and population genetic studies. In addition, future studies using genome-wide molecular markers and additional species from the continent, as well as sampling extinct species from the islands, will improve our knowledge about the origin and relationships of the endemic rodents of the Galápagos Islands.

Biografía del autor/a

Susette Castañeda-Rico, Smithsonian Institution / George Mason University

Center for Conservation Genomics / Postdoctoral Research Fellow

Sarah A. Johnson, George Mason University. Commission on Environmental Quality (TCEQ).

Commission on Environmental Quality (TCEQ) / Permit Coordinator

Scott A. Clement, Angelo State University

Department of Biology / Associate Professor

Robert C. Dowler, Angelo State University

Department of Biology / Professor - Curator of Mammals

Jesús E. Maldonado, Center for Conservation Genomics, Smithsonian Conservation Biology Institute.

Center for Conservation Genomics, Smithsonian Conservation Biology Institute / Research Geneticist

Cody W. Edwards, George Mason University. Smithsonian-Mason School of Conservation.

Smithsonian-Mason School of Conservation / Associate Professor and Associate Provost

Citas

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

Benavides, E., R. Baum, D. McClellan, and J. W. Sites Jr. 2007. Molecular phylogenetics of the lizard genus Microlophus (Squamata: Tropiduridae): aligning and retrieving indel signal from nuclear introns. Systematics Biology 56:776-797.

Best, T. L. 1988. Dipodomys spectabilis. Mammalian Species 311:1-10.

Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C-H. Wu, D. Xie, M. A. Suchard, A. Rambaut, and A. J. Drummond. 2014. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Computational Biology 10:e1003537.

Brosset, A. 1963. Statut actuel des mammiferes des iles GalaÌpagos. Mammalia 27:323- 338.

Cabrera, A. 1961. Catálogo de los mamíferos de América del Sur. Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’. Ciencias Zoologicas 4:309-732.

Caccone, A., J. P. Gibbs, V. Ketmaier, E. Suatoni, and J. R. Powell. 1999. Origin and evolutionary relationships of giant Galápagos tortoises. Proceedings of the National Academy of Science of the United States of America 96:223-228.

Christie, D. M., R. A. Duncan, A. R. McBirney, M. A. Richards, W. M. White, K. S. Harpp, and G. G. Fox. 1992. Drowned islands downstream from the Galápagos hotspot imply extended speciation times. Nature 355:246–248.

Clark, D. A. 1984. Native land mammals. Pp. 225-231 in Key environments: Galápagos (Perry, R. ed.). Pergamon Press. Oxford, U.K.

Clark, D. B. 1980. Population ecology of an endemic Neotropical island rodent: Oryzomys bauri of Santa Fe Island, Galapagos, Ecuador. Journal of Animal Ecology 49:185-198.

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

Deli, T., S. Fratini, L. Ragionieri, K. Said, N. Chatti, and C. D. Schubart. 2016. Phylogeography of the marbled crab Pachygrapsus marmoratus (Decapoda, Grapsidae) along part of the African Mediterranean coast reveals genetic homogeneity across the Siculo-Tunisian Strait versus heterogeneity across the Gibraltar Strait. Marine Biology Research 12:471-487.

Dexter, N., R. C. Dowler, J. P. Flanagan, S. Hart, M. A. Revelez, and T. E. Lee. 2004. The influence of Feral Cats Felis catus on the distribution and abundance of introduced and endemic Galapagos rodents. Pacific Conservation Biology 10:210-215.

do Prado, J. R., and A. R. Percequillo. 2018. Systematics studies of the genus Aegialomys Weksler et al., 2006. (Rodentia: Cricetidae: Sigmodontinae): Geography variation, species delimitation, and biogeography. Journal of Mammalian Evolution 25:71-118.

Dowler, R. C. 2015. Genus Nesoryzomys. Pp. 390-393 in Mammals of South America. Volume 2. (Patton, J. L., U. F. J. Pardiñas, and G. D’Elía, eds.). The University of Chicago Press. Chicago, U.S.A.

Dowler, R. C., and D. S. Carroll. 1996. The endemic rodents of Isla Fernandina: population status and conservation issues. Noticias de Galápagos 57:8-13.

Dowler, R. C., D. S. Carroll, and C. W. Edwards. 2000. Rediscovery of rodents (Genus Nesoryzomys) considered extinct in the GalaÌpagos Islands. Oryx 34:109-117.

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

Excoffier, L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology 13:853-864.

Fu, Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925.

Geist, D. 1984. On the emergence and submergence of the Galápagos islands. Noticias de Galápagos 56:5-9.

Geist, D., B. A. Diefenbach, D. J. Fornari, M. D. Kurz, K. Harpp, and J. Blusztajn. 2008. Construction of the GalaÌpagos platform by large submarine volcanic terraces. Geochemestry Geophysics Geosystems 9: doi:10.1029/2007GC001795.

Geist, D. J., H. Snell, H. Snell, C. Goddard, and M. D. Kurz. 2014. A paleogeographic model of the Galápagos Islands and biogeographical and evolutionary implications. Pp. 145-167 in The Galápagos A natural laboratory for earth sciences. (Harpp, K. S., E. Mittelstaedt, N. d’Ozouville, and D. W. Graham, eds.). John Wiley and Sons, Inc. Hoboken, U.S.A.

González-Ittig, R. E., G. R. Theiler, and C. N. Gardenal. 2002. A contribution to the subgeneric systematics of Oligoryzomys (Rodentia, Muridae) from Argentina by means of PCR-RFLP patterns of mitochondrial DNA. Biochemical Systematics and Ecology 30:23-33.

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

Harpending, H. C. 1994. Signature of ancient population-growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66:591-600.

Harpending, H., and A. Rogers. 2000. Genetic perspectives on human origins and differentiation. Annual Review of Genomics and Human Genetics 1:361-385.

Harpp, K.S., E. Mittelstaedt, N. d’Ozouville, and D. W. Graham (eds.). 2014. The Galápagos A natural laboratory for earth sciences. John Wiley and Sons, Inc. Hoboken, U.S.A.

Harris, D. B., S. D. Gregory, and D. W. Macdonald. 2006. Space invaders? A search for patterns underlying the coexistence of alien black rats and Galápagos rice rats. Oecologia 149:276-288.

Harris, D. B., and D. W. Macdonald. 2007. Population ecology of the endemic rodent Nesoryzomys swarthi in the tropical desert of the Galápagos Islands. Journal of Mammalogy 88:208-219.

Heller, E. 1904. Mammals of the Galápagos archipelago, exclusive of the Cetacea. Proceedings of the California Academy of Sciences 3:233-251.

Hendriks, K. P., G. Alciatore, M. Schilthuizen, and R. S. Etienne. 2019. Phylogeography of Bornean land snails suggests long-distance dispersal as a cause of endemism. Journal of Biogeography 46:1-13.

Hirota, T., Hirohata, T., Mashima H., Satoh, T., and Y. Obara. 2004. Population structure af large Japanese field mouse, Apodemus speciosus (Rodentia: Muridae), in suburban landscape, based on mitochondrial D-loop sequences. Molecular Ecology 13:3275-3282.

Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754-755.

Hutterer, R., and U. Hirsch. 1980. Ein neuer Nesoryzomys von der Insel Fernandina, Galápagos. Bonner Zoologische Beitrage 30:276-283.

Hutterer, R., and P. Oromí. 1993. La rata gigante de la Isla Santa Cruz, Galápagos: algunos datos y problemas. Resultados científicos del proyecto Galápagos: patrimonio de la humanidad. Museo de Ciencias Naturales, Tenerife (TFMC) 4:63-76.

IUCN (International Union for Conservation of Nature). 1996. IUCN Red List of Threatened Animals. IUCN, Gland, Switzerland.

IUCN (International Union for Conservation of Nature). 2019. The IUCN Red List of Threatened Species. International Union for Conservancy of Nature and Natural Resources. Version 2019-1. Available on http://www.iucnredlist.org. Downloaded on 05 June 2019.

Key, G., and E. Muñoz-Heredia. 1994. Distribution and current status of rodents in the Galápagos. Noticias de Galápagos 53:21-25.

Kizirian, D., A. Trager, M. A. Donnelly, and J. W. Wright. 2004. Evolution of Galápagos Island lava lizards (Iguania: Tropiduridae: Microlophus). Molecular Phylogenetics and Evolution 32:761-769.

Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A.Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.

Leigh, J. W., and D. Bryant. 2015. PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution 6:1110-1116.

Leite, R. N., S. O. Kolokotronis, F. C. Almeida, F. P. Werneck, D. S. Rogers, and M. Weksler. 2014. In the wake of invasion: tracing the historical biogeography of the South American Cricetid radiation (Rodentia, Sigmodontinae). PlosOne 9:1-12.

Losos, J. B., and R. E. Ricklefs. 2009. Adaptation and diversification on islands. Nature 457:830-836.

Losos, J. B. 2010. Adaptive radiation, ecological opportunity, and evolutionary determinism. The American Naturalist 175:623-639.

Machado, L. F., Y. L. R. Leite, A. U. Christoff, and L. G. Giugliano. 2014. Phlogeny and biogeography of tetraphodont rodents of the tribe Oryzomyini (Cricetidae: Sigmodontinae). Zoologica Scripta 43:119-130.

Merlen, G. 2014. Plate tectonics, evolution, and the survival of species: A modern day hotspot. Pp. 128-153 in The Galápagos A natural laboratory for earth sciences (Harpp, K. S., E. Mittelstaedt, N. d’Ozouville, and D. W. Graham, eds.). John Wiley and Sons, Inc. Hoboken, U.S.A.

Meserve, P. L. 1978. Water dependence in some Chilean arid zone rodents. Journal of Mammalogy 59:217-219.

Musser, G. G., and M. D. Carleton. 1993. Family Muridae. Pp. 501-755 in Mammal species of the world: a taxonomic and geographic reference (Wilson, D. E., and D. M. Reeder, eds.). 2nd ed. Smithsonian Institution Press. Washington, U.S.A.

Musser, G. G., and M. D. Carleton. 2005. Superfamily Muroidea. Pp. 894-1531 in Mammal species of the world: a taxonomic and geographic reference (Wilson, D. E., and D. M. Reeder, eds.). 3rd ed. Johns Hopkins University Press. Baltimore, U.S.A.

Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, USA.

Nowak, R.M. 1999. Walker’s Mammals of the World, 6th edn. The Johns Hopkins University Press. London, U.K.

Orr, R. T. 1938. A new rodent of the genus Nesoryzomys from the Galápagos Islands. Proceedings of the California Academy of Sciences Series 4 23:303-306.

Parada, A., U. F. J. Pardiñas, J. Salazar-Bravo, G. D’Elía, and R. E. Palma. 2013. Dating an impressive Neotropical radiation: Molecular time estimates for the Sigmodontinae (Rodentia) provide insights into its historical biogeography. Molecular Phylogenetics and Evolution 66:960-968.

Parent, C. E., A. Caccone, and K. Petren. 2008. Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B 363:3347-3361.

Patton, J. L. 1975. Biosystematics of the rodent fauna of the Galápagos Archipelago. American Philosophical Society Year Book 1975:352-353.

Patton, J. L. 1984. Genetical processes in the Galápagos. Biological Journal of the Linnean Society 21:97-111.

Patton, J. L., and M. S. Hafner. 1983. Biosystematics of the native rodents of the Galápagos Archipelago, Ecuador. Pp. 539-568 in Patterns of evolution in Galapagos organisms (Bowman, R. I., M. Berson, and A. E. Leviton, eds.). AAAS Pacific Division. San Francisco, U.S.A.

Peterson, R. L. 1966. Recent mammal records from the Galapagos Islands. Mammalia 30:441-445.

Philippe, H., H. Brinkmann, D. V. Lavrov, D. T. J. Littlewood, M. Manuel, G. Wörheide, and D. Baurain. 2011. Resolving difficult phylogenetic questions: Why more sequences are not enough. Plos Biology 9:1-10.

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

Rambaut A., A. J. Drummond, D. Xie, G. Baele, and M. A. Suchard. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901-904.

Ramos-Onsins S. E., and J. Rozas. 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19:2092-2100.

Ray, N., M. Currat, and L. Excoffier. 2003. Intra-Deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution 20:76-86.

Ribeiro, M. D. S., P. L. B. Da Rocha, L. A. F. Mendes, S. F. Perry, and E. S. De Oliveira. 2004. Physiological effects of short-term water deprivation in the South American sigmodontine rice rat Oligoryzomys nigripes and water rat Nectomys squamipes within a phylogenetic context. Canadian Journal of Zoology 82:1326-1335.

Robins, J. H., V. Tintinger, K. P. Aplin, M. Hingston, E. Matisoo-Smith, D. Penny, and S. D. Lavery. 2014. Rapid radiation and morphological similarity of New Guinean species. PlosOne 9:e107667.

Rodrigues, J. F. M., and J. A. F. Diniz-Filho. 2016. Ecological opportunities, habitat, and past climatic fluctuations influenced the diversification of modern turtles. Molecular Phylogenetics and Evolution 101:352-358.

Rogers, A. R., and H. C. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9:552-569.

Román-Palacios, C., and J. J. Wiens. 2018. The tortoise and the finch: Testing for island effects on diversification using two iconic Galápagos radiations. Journal of Biogeography 45:1701-1712.

Ronquist, F., and J. P. Huelsenbeck. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.

Rozas J., A. Ferrer-Mata, J. C. Sánchez-Del Barrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins, A. Sánchez-Gracia. 2017. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Molecular Biology and Evolution 34:3299-3302.

Slatkin M., and R. R. Hudson. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555-562.

Snell, H. M., P. A. Stone, and H. L. Snell. 1996. A summary of geographical characteristics of the Galápagos Islands. Journal Biogeography 23:619-624.

Steadman, D. W. 1985. Vertebrate paleontology of the Galápagos Islands. National Geographic Society Research Reports 20:717-724.

Steadman, D. W. 1986. Holocene Vertebrate Fossils from Isla Floreana, GalaÌpagos. Smithsonian contributions to zoology, Number 413, Smithsonian Institution Press. Washington, U.S.A.

Tajima, F. 1989a. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.

Tajima, F. 1989b. The effect of change in population size on DNA polymorphism. Genetics 123:597-601.

Urgoiti, J., Muñoz, A., Espelta, J. M., and R. Bonal. 2018. Distribution and space use of seed-dispersing rodents in central Pyrenees: implications for genetic diversity, conservation and plan recruitment. Integrative Zoology 13:307-3138.

Weksler, M. 2003. Phylogeny of Neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Molecular Phylogenetics and Evolution 29:331-349.

Weksler, M. 2006. Phylogenetic relationships of oryzomyine rodents (Muroidea: Sigmodontinae): separate and combined analysis of morphological and molecular data. Bulletin of the American Museum of Natural History 296:1-149.

Weksler, M., A. R. Percequillo, and R. S. Voss. 2006. Ten new genera of oryzomyine rodents (Muridae: Sigmodontinae). American Museum Novitates 3537:1-29.

Weksler, M., and A. R. Percequillo. 2011. Key to the genera of the tribe Oryzomyini (Rodentia: Cricetidae: Sigmodontinae). Mastozoología Neotropical 18:281-292.

Werner, R., K. Hoernle, P. van den Bogaard, C. Ranero, and R. von Huene. 1999. Drowned 14-m.y.-old GalaÌpagos Archipelago off the coast of Costa Rica: implications for tectonic and evolutionary models. Geology 27:499–502.

Wilke, T., R. Schultheiß, and C. Albrecht. 2009. A time goes by: A simple fool´s guide to molecular clock approaches in vertebrates. American Malacological Bulletin 27:25-45.

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2019-09-19

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