ORIGINAL ARTICLE
Geographical structure and cryptic lineages within common green iguanas, Iguana iguana
Catherine L. Stephen,
Víctor H. Reynoso,
William S. Collett,
Carlos R. Hasbun,
Jesse W. Breinholt,
Corresponding Author
Catherine L. Stephen
Department of Biology, Utah Valley University, Orem, UT, USA
Correspondence: Department of Biology, 800 West University Pkwy, MS 299, Utah Valley University, Orem, UT 84004, USA.
E-mail: [email protected]
Search for more papers by this authorVíctor H. Reynoso
Colección Nacional de Anfibios y Reptiles, Departamento de Zoología, Universidad Nacional Autónoma de México, Mexico, DF, México
Search for more papers by this authorWilliam S. Collett
Department of Biology, Utah Valley University, Orem, UT, USA
Search for more papers by this authorCarlos R. Hasbun
Fundación Zoológica de El Salvador, San Salvador, El Salvador
Search for more papers by this authorJesse W. Breinholt
Department of Biology, Brigham Young University, Provo, UT, USA
Search for more papers by this authorCatherine L. Stephen,
Víctor H. Reynoso,
William S. Collett,
Carlos R. Hasbun,
Jesse W. Breinholt,
Corresponding Author
Catherine L. Stephen
Department of Biology, Utah Valley University, Orem, UT, USA
Correspondence: Department of Biology, 800 West University Pkwy, MS 299, Utah Valley University, Orem, UT 84004, USA.
E-mail: [email protected]
Search for more papers by this authorVíctor H. Reynoso
Colección Nacional de Anfibios y Reptiles, Departamento de Zoología, Universidad Nacional Autónoma de México, Mexico, DF, México
Search for more papers by this authorWilliam S. Collett
Department of Biology, Utah Valley University, Orem, UT, USA
Search for more papers by this authorCarlos R. Hasbun
Fundación Zoológica de El Salvador, San Salvador, El Salvador
Search for more papers by this authorJesse W. Breinholt
Department of Biology, Brigham Young University, Provo, UT, USA
Search for more papers by this authorAbstract
Aim
Our aim was to investigate genetic structure in Neotropical populations of common green iguanas (Iguana iguana) and to compare that structure with past geological events and present barriers. Additionally, we compared levels of divergence between lineages within Iguana with those within closely related genera in the subfamily Iguaninae.
Location
Neotropics.
Methods
DNA sequence data were collected at four loci for up to 81 individuals from 35 localities in 21 countries. The four loci, one mitochondrial (ND4) and three nuclear (PAC, NT3, c-mos), were chosen for their differences in coalescent and mutation rates. Each locus was analysed separately to generate gene trees, and in combination in a species-level analysis.
Results
The pairwise divergence between Iguana delicatissima and I. iguana was much greater than that between sister species of Conolophus and Cyclura and non-sister species of Sauromalus, at both mitochondrial (mean 10.5% vs. 1.5–4%, respectively) and nuclear loci (mean 1% vs. 0–0.18%, respectively). Furthermore, divergences within I. iguana were equal to or greater than those for interspecific comparisons within the outgroup genera. Phylogenetic analyses yielded four strongly supported, geographically defined mitochondrial clades (3.8–5% divergence) within I. iguana. Three of the four clades were found using PAC (0.18–1.65% divergence) and two using NT3 (0.6% divergence) alone. The primary divergence, recovered in three polymorphic loci, was between individuals north and south of the Isthmus of Panama. The southern group was differentiated into clades comprising individuals on either side of the northern Andes, using both PAC and ND4.
Main conclusions
Deep genetic divergences were found within I. iguana that are congruent with past and current geological barriers. These divisions are greater than sister species comparisons in other Iguaninae genera, indicating the possible presence of cryptic species. Geological changes from the mid-Miocene through the Plio-Pleistocene have shaped the pattern of divergence in I. iguana. The uplift of the northern Andes presented a barrier between South American I. iguana populations by 4 Ma. Populations north of the Isthmus of Panama form a clade that is distinct from those to the south, and may have expanded northwards following the closing of the Isthmus of Panama 2.5 Ma.
Supporting Information
| Filename | Description |
|---|---|
| jbi2780-sup-0001-AppendixS1.xlsMS Excel, 43.5 KB | Appendix S1 Collection information for individuals in the subfamily Iguaninae included in the study and GenBank accession numbers for all haplotypes. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Alvarado, J., Ibarra, L., Suazo, I., Rodríguez, G. & Zamora, R. (1995) Reproductive characteristics of a green iguana (Iguana iguana) population of the west coast of Mexico. The Southwestern Naturalist, 40, 234–237.
- Antonelli, A., Nylander, J.A., Persson, C. & Sanmartín, I. (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the National Academy of Sciences USA, 106, 9749–9754.
- Bakhuis, W.L. (1982) Size and sexual differentiation in the lizard Iguana iguana on a semiarid island. Journal of Herpetology, 16, 322–325.
- Bellizzia, A. & Dengo, G. (1990) The Caribbean mountain system, northern South America; a summary. The geology of North America: the Caribbean region, Vol. H (ed. by G. Dengo and J.E. Case), pp. 167–175. Geological Society of America, Boulder, CO.
- Benítez-Malvido, J., Tapia, E.M., Suazo, I., Villaseñor, E. & Alvarado, J. (2003) Germination and seed damage in tropical dry forest plants ingested by iguanas. Journal of Herpetology, 37, 301–308.
- Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K. & Das, I. (2007) Cryptic species as a new window on diversity and conservation. Trends in Ecology and Evolution, 22, 148–155.
- Bock, B.C. (1984) Movement patterns relative to nesting site locations in a population of green iguanas (Iguana iguana) in Panama. PhD Thesis, University of Tennessee, Knoxville, TN.
- Bock, B.C. & McCracken, G.F. (1988) Genetic structure and variability in the green iguana (Iguana iguana). Journal of Herpetology, 22, 316–322.
- Brumfield, R.T. & Edwards, S.V. (2007) Evolution into and out of the Andes: a Bayesian analysis of historical diversification of Thamnophilus antshrikes. Evolution, 39, 346–367.
- Burnham, R.J. & Graham, A. (1999) The history of Neotropical vegetation: new developments and status. Annals of the Missouri Botanical Garden., 86, 546–589.
- Bush, M.B. (1994) Amazonian speciation: a necessarily complex model. Journal of Biogeography, 21, 5–17.
- Campbell, J. (1998) Amphibians and reptiles of northern Guatemala, the Yucatan, and Belize. University of Oklahoma Press, Norman, OK.
- Coates, A.G. (1997) Central America: a natural and cultural history. Yale University Press, New Haven, CT.
- Colborn, J., Crabree, R.E., Shalee, J.B., Pfeiler, E. & Bowen, B.W. (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution, 55, 807–820.
- Colbourne, J.K. & Hebert, P.D.N. (1996) The systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach. Philosophical Transactions of the Royal Society B: Biological Sciences, 351, 349–360.
- Conrad, J.L. & Norell, M.A. (2010) Cranial autapomorphies in two species of iguana (Iguanidae: Squamata). Journal of Herpetology, 44, 307–312.
- Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodriguez-Luna, E. & Sampaio, I. (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26, 64–81.
- Cracraft, J. & Prum, R.O. (1988) Patterns and processes of diversification: speciation and historical congruence in some Neotropical birds. Evolution, 42, 603–620.
- DeSalle, R., Egan, M.G. & Siddall, M. (2005) The unholy trinity: taxonomy, species delimitation, and DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1905–1916.
- Dugan, B.A. (1980) A field study of the social structure, mating system, and display behaviour of the green iguana. PhD Thesis, University of Tennessee, Knoxville, TN.
- Dunn, E.R. (1934) Notes on Iguana. Copeia, 1, 1–4.
10.2307/1436422 Google Scholar
- Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.
- Etheridge, R. (1982) Checklist of the iguanine and Malagasy iguanid lizards. Iguanas of the world: their behavior, ecology and conservation (ed. by G.M. Burghardt and A.S. Rand), pp. 7–37. Noyes Publishing, Park Ridge, NJ.
- Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611–2620.
- Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.
- Felsenstein, J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17, 368–376.
- Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
- Fowler, H.W. (1913) Amphibians and reptiles from Ecuador, Venezuela, and Yucatan. Proceedings of the Academy of Natural Sciences of Philadelphia, 65, 153–176.
- González, A.M., Brehm, A., Pérez, J.A., Maca-Meyer, N., Flores, C. & Cabrera, V.M. (2003) Mitochondrial DNA affinities at the Atlantic fringe of Europe. American Journal of Physical Anthropology, 120, 391–404.
- Greene, H., Burghardt, G.M., Dugan, B.A. & Rand, A.S. (1978) Predation and the defensive behavior of green iguanas (Reptilia, Lacertilia, Iguanidae). Journal of Herpetology, 12, 169–176.
- Gregory-Wodzicki, K. (2000) Uplift history of the central and northern Andes: a review. Geological Society of America Bulletin, 112, 1091–1105.
- Hallinan, T. (1920) Notes on the Canal Zone, Isthmus of Panama. Copeia, 83, 45–49.
10.2307/1437200 Google Scholar
- Haq, B.U., Hardenbol, J. & Vail, P.R. (1987) Chronology of fluctuating sea levels since the Triassic. Science, 235, 1156–1167.
- Harris, D.M. (1982) The phenology growth, and survival of the green iguana, Iguana iguana, in northern Colombia. Iguanas of the world: their behavior, ecology and conservation (ed. by G.M. Burghardt and A.S. Rand), pp. 150–161, Noyes Publishing, Park Ridge, NJ.
- Hasbun, C.R., Gomez, A., Kohler, G. & Lunt, D.H. (2005) Mitochondrial DNA phylogeography of the Mesoamerican spiny-tailed lizards (Ctenosaura quinquecarinata complex): historical biogeography, species status and conservation. Molecular Ecology, 14, 3095–3107.
- Haug, G.H., Tiedemann, R., Zahn, R. & Ravelo, A.C. (2001) Role of Panama uplift on oceanic freshwater balance. Geology, 29, 207–210.
- Heled, J. & Drummond, A.J. (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580.
- Henderson, R.W. (1974) Aspects of the ecology of the juvenile common iguana (Iguana iguana). Herpetologica, 30, 327–332.
- Henderson, R.W. & Hedges, S.B. (1995) Origin of West Indian populations of the geographically widespread boa Corallus enydris inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 4, 88–92.
- Heraty, J.M., Woolley, J.B., Hopper, K.R., Hawks, D.L., Kim, J. & Buffington, M. (2007) Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Molecular Phylogenetics and Evolution, 45, 480–493.
- Hollingsworth, B.D. (1998) The systematics of chuckwallas (Sauromalus) with a phylogenetic analysis of other iguanid lizards. Herpetological Monographs, 12, 38–191.
10.2307/1467020 Google Scholar
- Hollingsworth, B.D. (2004) The evolution of iguanas: an overview of relationships and a checklist of species. Iguanas: biology and conservation (ed. by A.C. Alberts, R.L. Carter, W.K. Hayes and E.P. Martins), pp. 19–44. University of California Press, Berkeley, CA.
- Hoogmoed, M.S. (1973) Notes on the herpetofauna of Surinam. Biogeographica, 4, 1–119.
- Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.
- Iturralde-Vinent, M.A. (2006) Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region. International Geology Review, 48, 791–827.
- Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801–1806.
- Kass, R.E. & Raftery, A.E. (1995) Bayes factors. Journal of the American Statistical Association, 90, 773–795.
- Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518.
- Klatau, M., Russo, C.A.M., Lazoski, C., Thorpe, J.P. & Sole-Cava, A.M. (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution, 53, 1414–1422.
- Lazell, J.D., Jr (1973) The lizard genus Iguana in the Lesser Antilles. Bulletin of the Museum of Comparative Zoology, 145, 1–28.
- Leaché, A.D. (2009) Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Systematic Biology, 58, 547–559.
- Makowsky, R., Chesser, J. & Risler, L.J. (2009) A striking lack of genetic diversity across the wide-ranging amphibian Gastrophryne carolinensis (Anura: Microhylidae). Genetica, 135, 169–183.
- Malone, C.L. & Davis, S.K. (2004) Genetic contributions to Caribbean iguana conservation. Iguanas: biology and conservation (ed. by A.C. Alberts, R.L. Carter, W.K. Hayes and E.P. Martins), pp. 45–57. University of California Press, Berkeley, CA.
- Malone, C.L., Wheeler, T., Taylor, J.T. & Davis, S.K. (2000) Phylogeography of the Caribbean rock iguana (Cyclura): implications for conservation and insights on the biogeographic history of the West Indies. Molecular Phylogenetics and Evolution, 17, 269–279.
- Malthora, A. & Thorpe, R.S. (2004) Maximizing information in systematic revisions: a combined molecular and morphological analysis of a cryptic green pitviper complex (Trimeresurus stejnegeri). Biological Journal of the Linnean Society, 82, 219–235.
- Marks, B.D., Hackett, S.J. & Capparella, A.P. (2002) Historical relationships among Neotropical lowland forest areas of endemism as determined by mitochondrial DNA sequence variation within the wedge-billed woodcreeper (Aves: Dendrocolaptidae: Glyphorynchus spirurus). Molecular Phylogenetics and Evolution, 24, 153–167.
- 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: Biological Sciences, 267, 1135–1141.
- Milá, B., Wayne, R.C., Fitze, P. & Smith, T.B. (2009) Divergence with gene flow and fine-scale phylogeographical structure in the wedge-billed woodcreeper, Glyphorynchus spirurus, a Neotropical rainforest bird. Molecular Ecology, 18, 2979–2995.
- Moritz, C. (1994) Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology and Evolution, 9, 373–375.
- Müller, H. (1968) Untersuchungen über Wachstum und Altersverteilung einer Population des Grünen Leguans Iguana iguana iguana L. (Reptilia: Iguanidae). Instituto Colombo-Alemán Investigacion Científica Punta de Betín, 2, 57–65.
- Noonan, B.P. & Chippindale, P.T. (2006a) Dispersal and vicariance: the complex evolutionary history of boid snakes. Molecular Phylogenetics and Evolution, 40, 347–358.
- Noonan, B.P. & Chippindale P.T. (2006b) Vicariant origin of Malagasy reptiles supports Late Cretaceous Antarctic land bridge. The American Naturalist, 168, 730–741.
- Norell, M.A. (1989) Late Tertiary fossil lizards of the Anza-Borrego Desert, California. Contributions in Science, No. 414. Natural History Museum of Los Angeles County, Los Angeles, CA.
- Pasachnik, S.A., Fitzpatrick, B.M., Near, T.J. & Echternacht, A.C. (2008) Gene flow between an endangered endemic iguana, and its wide spread relative, on the island of Utila, Honduras: when is hybridization a threat? Conservation Genetics, 10, 1247–1254.
- Patton, J.L. & Smith, M.F. (1992) MtDNA phylogeny of Andean mice: a test of diversification across ecological gradients. Evolution, 46, 174–183.
- Peppers, L.L. & Bradley, R.D. (2000) Cryptic speciation in Sigmodon hispidus: evidence from DNA sequences. Journal of Mammalogy, 81, 332–343.
- Petren, K. & Case, T.J. (1997) A phylogenetic analysis of body size evolution and biogeography in chuckwallas (Sauromalus) and other iguanines. Evolution, 51, 206–219.
- Pfenninger, M. & Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BioMed Central Evolutionary Biology, 7, 1–6.
- Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
- Prance, G.T. (1982) A review of the phytogeographic evidences for Pleistocene climate changes in the Neotropics. Annals of the Missouri Botanical Garden, 69, 594–624.
- de Quieroz, K. (1987) Phylogenetic systematics of iguanine lizards: a comparative osteological study. University of California Publications in Zoology 118. University of California Press, Berkeley.
10.5962/bhl.title.4857 Google Scholar
- Rambaut, A. & Drummond, A.J. (2007) Tracer version 1.4. Available at: http://beast.bio.ed.ac.uk/Tracer.
- Rand, S.A. (1957) Notes on amphibians and reptiles from El Salvador. Fieldiana Zoology, 34, 505–534.
- Rand, S.A., Dugan, B.A., Monteza, H. & Vianda, D. (1990) The diet of a generalized folivore: Iguana iguana in Panama. Journal of Herpetology, 24, 211–214.
- Retallack, G.J. & Kirby, M.X. (2007) Middle Miocene global change and paleogeography of Panama. Palaios, 22, 667–679.
- Rivas, J.A., Molina, C.R. & Avila, T.M. (1998) Iguana iguana (green iguana). Juvenile predation. Herpetological Review, 29, 238–239.
- Rodda, G.H. (1992) The mating behavior of Iguana iguana. Smithsonian Contributions to Zoology No. 534. Smithsonian Institution, Washington, DC.
- Sanderson, M.J. & Donoghue, M.J. (1989) Patterns of variation in levels of homoplasy. Evolution, 43, 1781–1795.
- Sexton, O.J. (1975) Black vultures feeding on iguana eggs in Panama. American Midland Naturalist, 93, 463–468.
- Sites, J.W., Jr, Davis, S.K., Guerra, T., Iverson, J.B. & Snell, H.L. (1996) Character congruence and phylogenetic signal in molecular and morphological data sets: a case study in the living iguanas (Squamata, Iguanidae). Molecular Biology and Evolution, 13, 1087–1105.
- Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
- Starrett, J. & Hedin, M. (2007) Multilocus genealogies reveal multiple cryptic species and biogeographical complexity in the California turret spider Antrodiaetus riversi (Mygalomorphae, Antrodiatidae). Molecular Ecology, 16, 583–604.
- Stephen, C.L., Pasachnik, S., Reuter, A., Mosig, P., Ruyle, L. & Fitzgerald, L. (2011) Survey of status, trade, and exploitation of Central American iguanas. United States Fish and Wildlife Services, Washington, DC.
- Suchard, M.A., Weiss, R.E. & Sinsheimer, J.S. (2001) Bayesian selection of continuous-time Markov chain evolutionary models. Molecular Biology and Evolution, 18, 1001–1013.
- Swanson, P.L. (1950) The iguana Iguana iguana iguana (L). Herpetologica, 6, 187–193.
- Swofford, D.L. (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0. Sinauer Associates, Sunderland, MA.
- Toews, D.P. & Irwin, D.E. (2008) Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses. Molecular Ecology, 23, 2691–2705.
- Torres-Carvajal, O. & de Queiroz, K. (2009) Phylogeny of hoplocercine lizards (Squamata: Iguania) with estimates of relative divergence times. Molecular Phylogenetics and Evolution, 50, 31–43.
- Valdivieso, D. & Tamsitt, J.R. (1963) A checklist and key to the amphibian and reptiles of Providencia and San Andres. Caribbean Journal of Science, 3, 77–79.
- Van Denburgh, J. (1898) Reptiles from Sonora, Sinaloa, and Jalisco, Mexico, with a description of a new species of Sceloporus. Proceedings of the Academy of Natural Science of Philadelphia, 1897, 460–464.
- Venegas-Anaya, M., Crawford, A.J., Galván, A.H.E., Sanjur, O.I., Densmore, L.D., III & Bermingham, E. (2008) Mitochondrial DNA phylogeography of Caiman crocodilus in Mesoamerica and South America. Journal of Experimental Zoology, 309A, 614–627.
- Wertheim, J.O., Sanderson, M.J., Worobey, M. & Bjork, A. (2010) Relaxed molecular clocks, the bias-variance trade-off, and the quality of phylogenetic inference. Systematic Biology, 59, 1–8.
- Wiens, J.J. & Hollingsworth, B.D. (2000) War of the iguanas: conflicting molecular and morphological phylogenies and long branch attraction in iguanid lizards. Systematic Zoology, 49, 143–159.
- Wilcox, T.P., Hugg, L., Zeh, J.A. & Zeh, D.W. (1997) Mitochondrial DNA sequencing reveals extreme genetic differentiation in a cryptic species complex of Neotropical pseudoscorpions. Molecular Phylogenetics and Evolution, 7, 208–216.
- Witt, J.D.S. & Hebert, P.D.N. (2000) Cryptic species diversity and evolution in the amphipod genus Hyalella within central glaciated North America: a molecular phylogenetic approach. Canadian Journal of Fisheries and Aquatic Sciences, 57, 687–698.
- Wüster, W., Ferguson, J.E., Quijada-Mascareñas, J.A., Pook, C.E., da Graça Salomão, M. & Thorpe, R.S. (2005) Tracing an invasion: landbridges, refugia, and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Molecular Ecology, 14, 1095–1108.
- 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.
- Zeh, D.W., Zeh, J.A. & Bonilla, M.M. (2003) Phylogeography of the giant harlequin beetle (Acrocinus longimanus). Journal of Biogeography, 30, 747–753.
