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Article
Published: 2016-07-15

A cryptic palm-pitviper species (Squamata: Viperidae: Bothriechis) from the Costa Rican highlands, with notes on the variation within B. nigroviridis 

Department of Biology, University of Central Florida, 4000 Central Florida Blvd, Orlando, FL 32816, USA.
Department of Biology, University of Central Florida, 4000 Central Florida Blvd, Orlando, FL 32816, USA.
Department of Biology, 501 S. Nedderman Drive, University of Texas at Arlington, Arlington, TX 76019, USA.
Instituto Clodomiro Picado, Facultad de Microbiología, Universidad de Costa Rica, and Palo Verde Biological Station, Organization for Tropical Studies, San José, Costa Rica.
Department of Biology, University of Central Florida, 4000 Central Florida Blvd, Orlando, FL 32816, USA.
Reptilia Bothriechis nubestris Costa Rica Middle America new species snake Squamata taxonomy Viperidae

Abstract

Middle America is one of the most biodiverse regions in the world, harboring an exceptional number of rare and endemic species. This is especially true of Middle American cloud forests, where montane specialists occupy restricted, high-elevation ranges making them attractive candidates for investigating historical biogeography and speciation. One such highland-restricted species, the black speckled palm-pitviper (Bothriechis nigroviridis), occupies the Central, Tilarán, and Talamanca Cordilleras in Costa Rica and Panama. In this study, we investigate the genetic and morphological variation among populations of B. nigroviridis by inferring a multilocus phylogeny (21 individuals) and analyzing meristic scale characters with a principal component analysis (64 individuals). We find B. nigroviridis sensu stricto to be composed of two deeply divergent lineages, one with a restricted range in the northern and central Cordillera Talamanca and the other ranging throughout the Central, Tilarán, and Talamanca Cordilleras. Furthermore, these two lineages are morphologically distinct, with previously unrecognized differences in several characters allowing us to name and diagnose a new species B. nubestris sp. nov. We also examine the genetic and morphological variation within B. nigroviridis and discuss biogeographic hypotheses that may have led to the diversification of Bothriechis lineages.

 

References

  1. Abratis, M. & Wörner, G. (2001) Ridge collision, slab-window formation, and the flux of Pacific asthenosphere into the Caribbean realm. Geology, 29, 127–130.
    http://dx.doi.org/10.1130/0091-7613(2001)029<0127:RCSWFA>2.0.CO;2

    Arbogast, B.S. & Kenagy, G.J. (2001) Comparative phylogeography as an integrative approach to historical biogeography. Journal of Biogeography, 28, 819–825.
    http://dx.doi.org/10.1046/j.1365-2699.2001.00594.x

    Arévalo, E., Davis, S.K. & Sites, J.W. Jr. (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Systematic Biology, 43, 387–418.
    http://dx.doi.org/10.1093/sysbio/43.3.387

    Bacon, C.D., Silvestro, D., Jaramillo, C., Smith, B.T., Chakrabarty, P. & Antonelli, A. (2015) Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the National Academy of Sciences of the United States of America, 112, 6110–6115.
    http://dx.doi.org/10.1073/pnas.1423853112

    Bagley, J.C. & Johnson, J.B. (2014) Phylogeography and biogeography of the lower Central American Neotropics: diversification between two continents and between two seas. Biological Reviews of the Cambridge Philosophical Society, 89, 767–790.
    http://dx.doi.org/10.1111/brv.12076

    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–55.
    http://dx.doi.org/10.1016/j.tree.2006.11.004

    Brandley, M.C., Schmitz, A. & Reeder, T.W. (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology, 54, 373–390.
    http://dx.doi.org/10.1080/10635150590946808

    Burbrink, F.T., Lawson, R. & Slowinski, J.B. (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): A critique of the subspecies concept. Evolution, 54, 2107–2118.
    http://dx.doi.org/10.1554/0014-3820(2000)054[2107:MDPOTP]2.0.CO;2

    Campbell, J.A. (1999) Distribution patterns of amphibians in Middle America. In: Duellman, W.E. (Eds.), Distribution Patterns of Amphibians: A Global Perspective. The Johns Hopkins University Press, Baltimore and London, pp. 111–209.

    Campbell, J.A. & Lamar, W.W. (2004) Venomous Reptiles of the Western Hemisphere, Vol 2. Cornell University Press. Ithaca, USA, 976 pp.

    Castoe, T.A & Parkinson, C.L. (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Molecular Phylogenetics and Evolution, 39, 91–110.
    http://dx.doi.org/10.1016/j.ympev.2005.12.014

    Castoe, T.A., Daza, J.M., Smith, E.N., Sasa, M.M., Kuch, U., Campbell, J.A., Chippindale, P.T. & Parkinson, C.L. (2009) Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. Journal of Biogeography, 36, 88–103.
    http://dx.doi.org/10.1111/j.1365-2699.2008.01991.x

    Castoe, T.A., Doan, T.M. & Parkinson, C.L. (2004) Data partitions and complex models in Bayesian analysis: the phylogeny of gymnophthalmid lizards. Systematic Biology, 53, 448–469.
    http://dx.doi.org/10.1080/10635150490445797

    Crother, B.I., Campbell, J.A. & Hillis, D.M. (1992) Phylogeny and historical biogeography of the palm-pitvipers, genus Bothriechis: biochemical and morphological evidence. In: Campbell, J.A. & Brodie, Jr., E.D. (Eds.), Biology of the Pitvipers. Selva. Tyler, USA, pp. 1–19.

    Daza, J.M., Castoe, T.A. & Parkinson, C.L. (2010) Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America. Ecography, 33, 343–354.
    http://dx.doi.org/10.1111/j.1600-0587.2010.06281.x

    Daza, J.M., Smith, E.N., Páez, V.P. & Parkinson, C.L. (2009) Complex evolution in the Neotropics: The origin and diversification of the widespread genus Leptodeira (Serpentes: Colubridae). Molecular Phylogenetics and Evolution, 53, 653–667.
    http://dx.doi.org/10.1016/j.ympev.2009.07.022

    Driese, S.G., Orvis, K.H., Horn, S.P., Li, Z.H. & Jennings, D.S. (2007) Paleosol evidence for Quaternary uplift and for climate and ecosystem changes in the Cordillera de Talamanca, Costa Rica. Palaeogeography, Palaeoclimatology, Palaeoecology, 248, 1–23.
    http://dx.doi.org/10.1016/j.palaeo.2006.11.013

    Dzierma, Y., Rabbel, W., Thorwart, M.M., Flueh, E.R., Mora, M.M. & Alvarado, G.E. (2011) The steeply subducting edge of the Cocos Ridge: Evidence from receiver functions beneath the northern Talamanca Range, south-central Costa Rica. Geochemistry, Geophysics, Geosystems, 12, 1–25.
    http://dx.doi.org/10.1029/2010GC003477

    Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
    http://dx.doi.org/10.1093/nar/gkh340

    Fernández, J., Lomonte, B., Sanz, L., Angulo, Y., Gutiérrez, J.M. & Calvete, J.J. (2010) Snake venomics of Bothriechis nigroviridis reveals extreme variability among palm pitviper venoms: Different evolutionary solutions for the same trophic purpose. Journal of Proteome Research, 9, 4234–4241.
    http://dx.doi.org/10.1021/pr100545d

    Funk, J., Mann, P., McIntosh, K. & Stephens, J. (2009) Cenozoic tectonics of the Nicaraguan depression, Nicaragua, and Median Trough, El Salvador, based on seismic-reflection profiling and remote-sensing data. Bulletin of the Geological Society of America, 121, 1491–1521.
    http://dx.doi.org/10.1130/B26428.1

    Garcia-Paris, M., Good, D.A., Parra-Olea, G. & Wake, D.B. (2000) Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proceedings of the National Academy of Sciences of the United States of America, 97, 1640–1647.
    http://dx.doi.org/10.1073/pnas.97.4.1640

    García-Rodríguez, A., Chaves, G., Benavides-Varela, C. & Puschendorf, R. (2012) Where are the survivors? Tracking relictual populations of endangered frogs in Costa Rica. Diversity and Distributions, 18, 204–212.
    http://dx.doi.org/10.1111/j.1472-4642.2011.00862.x

    Gazel, E., Carr, M.J., Hoernle, K., Feigenson, M.D., Szymanski, D., Hauff, F. & Van Den Bogaard, P. (2009) Galapagos-OIB signature in southern Central America: Mantle refertilization by arc-hot spot interaction. Geochemistry, Geophysics, Geosystems, 10, 1–32.
    http://dx.doi.org/10.1029/2008GC002246

    Groth, J.G. & Barrowclough, G. (1999) Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Molecular Phylogenetics and Evolution, 12, 115–123.
    http://dx.doi.org/10.1006/mpev.1998.0603

    Gutberlet, R.L. Jr. & Campbell, J.A. (2001) Generic recognition for a neglected lineage of South American pitvipers (Squamata: Viperidae: Crotalinae) with the description of a new species from the Colombian Chocó. American Museum Novitates, 31, 323–338.
    http://dx.doi.org/10.1206/0003-0082(2001)316<0001:grfanl>2.0.co;2

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.
    http://dx.doi.org/10.1093/bioinformatics/17.8.754

    Jadin, R.C., Townsend, J.H., Castoe, T.A. & Campbell, J.A. (2012) Cryptic diversity in disjunct populations of Middle American montane pitvipers: A systematic reassessment of Cerrophidion godmani. Zoologica Scripta, 41, 455–470.
    http://dx.doi.org/10.1111/j.1463-6409.2012.00547.x

    Köhler, G., Dehling, D.M. & Köhler, J. (2010) Cryptic species and hybridization in the Anolis polylepis complex, with the description of a new species from the Osa Peninsula, Costa Rica (Squamata: Polychrotidae). Zootaxa, 38, 23–38.

    Lachniet, M.S. & Seltzer, G.O. (2002) Late Quaternary glaciation of Costa Rica. Bulletin of the Geological Society of America, 114, 547–558.
    http://dx.doi.org/10.1130/0016-7606(2002)114<0922:LQGOCR>2.0.CO;2

    Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
    http://dx.doi.org/10.1093/molbev/mss020

    Lomonte, B., Mora-Obando, D., Fernández, J., Sanz, L., Pla, D., Gutiérrez, J.M. & Calvete, J.J. (2015) First crotoxin-like phospholipase A2 complex from a New World non-rattlesnake species: Nigroviriditoxin, from the arboreal Neotropical snake Bothriechis nigroviridis. Toxicon, 93, 144–154.
    http://dx.doi.org/10.1016/j.toxicon.2014.11.235

    Lunt, D.J., Valdes, P.J., Haywood, A. & Rutt, I.C. (2008) Closure of the Panama Seaway during the Pliocene: Implications for climate and Northern Hemisphere glaciation. Climate Dynamics, 30, 1–18.
    http://dx.doi.org/10.1007/s00382-007-0265-6

    Marshall, J.S. (2007). The geomorphology and physiographic provinces of Central America. In: Bundschuh, J. & Alvarado, G.E. (Eds.), Central America: Geology, Resources and Hazards. CRC Press. Boca Raton, USA, pp. 1–51.
    http://dx.doi.org/10.1201/9780203947043.pt2

    Marshall, J.S., Idleman, B.D., Gardner, T.W. & Fisher, D.M. (2003) Landscape evolution within a retreating volcanic arc, Costa Rica, Central America. Geology, 31, 419–422.
    http://dx.doi.org/10.1130/0091-7613(2003)031<0419:LEWARV>2.0.CO;2

    Martin, A.P. & Bermingham, E. (2000) Regional endemism and cryptic species revealed by molecular and morphological analysis of a widespread species of Neotropical catfish. Proceedings of the Royal Society B, 267, 1135–1141.
    http://dx.doi.org/10.1098/rspb.2000.1119

    Miller, K.B., Bergsten, J. & Whiting, M.F. (2009) Phylogeny and classification of the tribe Hydaticini (Coleoptera: Dytiscidae): Partition choice for Bayesian analysis with multiple nuclear and mitochondrial protein-coding genes. Zoologica Scripta, 38, 591–615.
    http://dx.doi.org/10.1111/j.1463-6409.2009.00393.x

    Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G. A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–8.
    http://dx.doi.org/10.1038/35002501

    O'Dea, A., Hoyos, N., Rodríguez, F., Degracia, B. & De Gracia, C. (2012) History of upwelling in the tropical eastern pacific and the paleogeography of the Isthmus of Panama. Palaeogeography, Palaeoclimatology, Palaeoecology, 348, 59–66.
    http://dx.doi.org/10.1016/j.palaeo.2012.06.007

    Parkinson, C.L. (1999) Molecular systematics and biogeographical history of pitvipers as determined by mitochondrial ribosomal DNA sequences. Copeia, 1999, 576–586.
    http://dx.doi.org/10.2307/1447591

    R Core Team. (2015) R: A Language and Environment for Statistical Computing. Ver 3.2. R Foundation for Statistical Computing. Vienna: Austria. Available from: www.R-project.org/ (Acessed 13 Jul. 2016)

    Rambaut, A., Suchard, M. & Drummond, A. (2013) Tracer v1.5. Available via http://tree.bio.ed.ac.uk/software/tracer/ (Acessed 13 Jul. 2016)

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
    http://dx.doi.org/10.1093/bioinformatics/btg180

    Sanders, K.L., Malhotra, A. & Thorpe, R.S. (2006) Combining molecular, morphological and ecological data to infer species boundaries in a cryptic tropical pitviper. Biological Journal of the Linnean Society, 87, 343–364.
    http://dx.doi.org/10.1111/j.1095-8312.2006.00568.x

    Savage, J. (1982) The enigma of the Central American herpetofauna: dispersals or vicariance? Annals of the Missouri Botanical Garden, 69, 464–547.
    http://dx.doi.org/10.2307/2399082

    Savage, J.M. (2002) The Amphibians and Reptiles of Costa Rica: A Herpetofauna Between Two Continents, Between Two Seas. University of Chicago Press. Chicago, USA, 954 pp.

    Savage, J.M. & Lahanas, P.N. (2008) A new species of colubrid snake (genus Urotheca) from the Cordillera de Talamanca of Costa Rica. Copeia, 1989, 892–896.
    http://dx.doi.org/10.2307/1445974

    Solórzano, A., Gómez, L.D., Monge-Nájera, J. & Crother, B.I. (1998) Redescription and validation of Bothriechis supraciliaris (Serpentes: Viperidae). Revista de Biologia Tropical, 46, 453–462.

    Streicher, J.W., Crawford, A.J. & Edwards, C.W. (2009) Multilocus molecular phylogenetic analysis of the montane Craugastor podiciferus species complex (Anura: Craugastoridae) in isthmian Central America. Molecular Phylogenetics and Evolution, 53, 620–630.
    http://dx.doi.org/10.1016/j.ympev.2009.07.011

    Taggart, T.W., Crother, B.I. & White, M.E. (2001) Palm-Pitviper (Bothriechis) phylogeny, mtDNA, and consilience. Cladistics, 17, 355–370.
    http://dx.doi.org/10.1111/j.1096-0031.2001.tb00130.x

    Townsend, J.H., Medina-Flores, M., Wilson, L.D., Jadin, R.C. & Austin, J.D. (2013) A relict lineage and new species of green palm-pitviper (Squamata, Viperidae, Bothriechis) from the Chortís Highlands of Mesoamerica. ZooKeys, 298, 77–106.
    http://dx.doi.org/10.3897/zookeys.298.4834

    Venegas-Anaya, M., Crawford, A.J., Escobedo Galván, A.H., Sanjur, O.I., Densmore, L.D. & Bermingham, E. (2008) Mitochondrial DNA phylogeography of Caiman crocodilus in MesoAmerica and South America. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 309, 614–627.
    http://dx.doi.org/10.1002/jez.502

    Zamudio, K.R. & Greene, H.W. (1997) Phylogeography of the bushmaster (Lachesis muta: Viperidae): implications for neotropical biogeography, systematics, and conservation. Biological Journal of the Linnean Society, 62, 421–442.
    http://dx.doi.org/10.1006/bijl.1997.0162