Pan American Health Organization, 2006. Regional Strategic Plan for Malaria in the Americas 2006–2010. Washington, DC: Pan American Health Organization.
Ministerio Nacional de Salud de Panamá, 2007. Análisis de la Situación de Malaria en Panamá. Boletín Epidemiológico. Available at: http://www.minsa.gob.pa. Accessed May 4, 2009.
Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE, 2008. Species composition and distribution of adult Anopheles (Diptera: Culicidae) in Panama. J Med Entomol 45: 841–851.
Calzada EJ, Samudio F, Bayard V, Obaldia N, De Mosca IB, Pascale JM, 2009. Revising antimalarial drug policy in Central America: experience of Panama. Trans R Soc Trop Med Hyg 102: 694–698.
Loaiza J, Scott M, Bermingham E, Rovira J, Conn J, 2009. Short report: Anopheles darlingi in Panama. Am J Trop Med Hyg 81: 23–26.
Lehmann T, Licht M, Elissa N, Maega BT, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA, 2003. Population structure of Anopheles gambiae in Africa. J Hered 94: 133–147.
Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Povoa MM, Padilla N, Nicole LA, Conn JE, 2008. Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol 8: 3.
Walton C, Handley JM, Tun-Lin W, 2000. Population structure and population history of Anopheles dirus mosquitoes in Southeast Asia. Mol Biol Evol 17: 962–974.
Mirabello L, 2007. Molecular Population Genetics of the Malaria Vector Anopheles darlingi throughout Central and South America using Mitochondrial, Nuclear and Microsatellites Markers. Ph.D. Thesis. Albany, NY: University at Albany.
O'Loughlin SM, Okabayashi T, Honda M, Kitazoe Y, Kishino H, Somboon P, Sochantha T, Nambanya S, Saikia PK, Dev V, Walton C, 2008. Complex population history of two Anopheles dirus mosquito species in south Asia suggests the influence of Pleistocene climate change rather than human-mediated effects. J Evol Biol 21: 1555–1569.
Faran ME, 1980. Mosquito studies (Diptera: Culicidae) XXXIV. A revision of the Albimanus section of the subgenus Nyssorhynchus of Anopheles, contrib. Am Entomol Inst 15: 1–215.
Breeland SG, 1972. Studies on the ecology of Anopheles albimanus. Am J Trop Med Hyg 21: 751–754.
Hobbs J, Sexton J, St. Jean Y, Jacques J, 1986. The biting and resting behavior of Anopheles albimanus in northern Haiti. J Am Mosq Control Assoc 2: 150–153.
Beach RF, Mills D, Collins FH, 1989. Structure of ribosomal DNA in Anopheles albimanus (Diptera: Culicidae). Ann Entomol Soc Am 81: 641–648.
Narang SK, Seawright JA, Suarez MF, 1991. Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosq Control Assoc 7: 337–345.
De Merida AM, De Mata MP, Molina E, Porter CH, Black WC, 1995. Variation in ribosomal DNA intergenic spacers among populations of Anopheles albimanus in South and Central America. Am J Trop Med Hyg 53: 469–477.
Collins WE, Skinner JC, Warren M, Richardson B, 1976. Studies on human malaria in Aotus monkeys. VII. Comparative infectivity of two strains of Plasmodium vivax to Anopheles freeborni, An. maculatus, and four strains of An. albimanus. J Parasitol 62: 190–194.
Frederickson EC, 1993. Bionomics and Control of Anopheles albimanus. Washington, DC: Pan American Health Organization, Pan American Sanitary Bureau Regional Office of the World Health Organization.
Grieco JP, Achee NL, Roberts DR, Andre RG, 2005. Comparative susceptibility of three species of Anopheles from Belize, Central America, to Plasmodium falciparum (Nf-54). J Am Mosq Control Assoc 21: 279–290.
Achee NA, Achee N, Grieco JP, Andre RG, Rejmankova E, Roberts DR, 2007. A mark release-recapture study to define the flight behaviours of Anopheles vestitipennis and An. albimanus in Belize, Central America. J Am Mosq Control Assoc 3: 276–282.
De Merida AM, Palmieri M, Yurrita M, Molina A, Molina E, Black WC, 1999. Mitochondrial DNA variation among Anopheles albimanus populations. Am J Trop Med Hyg 6: 230–239.
Molina-Cruz A, De Merida AM, Mills K, Rodriguez F, Schoua C, Yurrita MM, Molina E, Palmieri M, William CB, 2004. Gene flow among Anopheles albimanus populations in Central America, South America, and the Caribbean assessed by microsatellites and mitochondrial DNA. Am J Trop Med Hyg 71: 350–359.
Conn JE, Mirabello L, 2007. The biogeography and population genetics of neotropical vector species. Heredity 99: 245–256.
Fairley TL, Renaud TM, Conn JE, 2000. Effects of local geographic barriers and latitude on population structure in Anopheles punctipennis (Diptera: Culicidae). J Med Entomol 37: 754–760.
Mirabello L, Conn JE, 2006. Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity 96: 311–321.
Wilkerson RC, Strickman D, 1990. Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J Am Mosq Control Assoc 6: 7–34.
Lunt DH, Zhang DX, Szymura JM, Hewitt GM, 1996. The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5: 153–165.
Swofford DL, 2003. PAUP (Phylogenetic Analysis Using Parsimony) and Other Methods, Version 4. Sunderland, MA: Sinauer Associates.
Maddison WP, Maddison DR, 1997. MacClade: Analysis of Phylogeny and Character Evolution, Version 3.07. Sunderland, MA: Sinauer Associates.
Tamura K, Dudley J, Nei M, Kumar S, 2007. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
Clement M, Posada D, Crandall KA, 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657–1659.
Posada D, Crandall KA, Templeton AR, 2000. GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9: 487–488.
Crandall KA, Templeton AR, 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134: 959–969.
Uthicke S, Benzie JAH, 2003. Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holoturoidea) populations from the Indo-Pacific. Mol Ecol 12: 2635–2648.
Excoffier L, Laval G, Schmeider S, 2005. Arlequin (version 3.0): an integrated software package for population genetic data analysis. Evol Bioinform Online 1: 47–50.
Mantel N, 1967. The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209–220.
Jensen J, Bohonak AJ, Kelley ST, 2005. Isolation by distance, web service. BMC Genet 6: 13.
Tajima F, 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics 123: 585–595.
Fu YX, Li WH, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.
Fu YX, 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.
Ramos-Onsins SE, Rozas J, 2002. Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092–2100.
Kimura M, 1983. The Neutral Theory of Molecular Evolution. Cambridge, England: Cambridge University Press.
Rozas J, Sanchez-Del Rio JC, Messeguer X, Rozas R, 2003. DnaSP, DNA polymorphism analyses by the coalescence and other methods. Bioinformatics 19: 2496–2497.
Nei M, 1987. Molecular Evolutionary Genetics. New York: Columbia University Press.
Harpending HC, Sherry ST, Rogers AR, Stoneking M, 1993. The genetic structure of ancient human populations. Curr Anthropol 34: 483–496.
Rogers AR, 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49: 608–615.
Tamura K, Nei M, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512–526.
Castelloe J, Templeton AR, 1994. Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phyl Evol 3: 102–113.
Powell JR, Caccone A, Amato GD, Yoon C, 1986. Rate of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83: 9090–9093.
Mirabello L, Conn JE, 2008. Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol 22: 109–119.
Conn JE, Vineis JH, Bollback JP, Onyabe DY, Wilkerson RC, Póvoa MM, 2006. Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg 74: 798–806.
Scarpassa VM, Conn JE, 2007. Population genetic structure of the major malaria vector Anopheles darlingi (Diptera: Culicidae) from the Brazilian Amazon, using microsatellite markers. Mem Inst Oswaldo Cruz 102: 319–327.
Conn J, Mitchell SE, Cockburn AF, 1998. Mitochondrial DNA analysis of the neotropical malaria vector Anopheles nuneztovari. Genome 41: 313–327.
Telles MP, Diniz-Filho JA, 2005. Multiple Mantel test and isolation by distance, taking into account long-term historical divergence. Genet Mol Res 4: 742–748.
Trapido H, 1952. Modified response of Anopheles albimanus to DDT residual house spraying in Panama. Am J Trop Med Hyg 15: 853–861.
Zink RM, Barrowclough GF, 2008. Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17: 2107–2121.
Templeton AR, 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7: 381–397.
Kolbe JJ, Glor RE, Schettino LR, Lara AD, Larson A, Losos JB, 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177–181.
Gonzáles C, Urrego LE, Martínez JI, 2006. Late quaternary vegetation and climate change in the Panama basin: palynological evidence from marine cores ODP 677 and TR 163-38. PALAEO 234: 62–80.
Golik A, 1968. History of the Holocene transgression in the Gulf of Panama. J Geol 76: 497–507.
Bermingham E, Martin AP, 1998. Comparative mtDNA phylogeography of neotropical fresh water fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol 7: 499–517.
Zeh JA, Zeh DW, Bonilla MM, 2003. Phylogeography of the harlequin beetle-riding pseudoscorpion and the rise of the Isthmus of Panama. Mol Ecol 12: 2759–2769.
Weigt LA, Crawford AJ, Stanley Rand A, Ryan M, 2005. Biogeography of the tungara frog, Physalaemus pustulosus: a molecular perspective. Mol Ecol 14: 3857–3876.
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The micro-geographic structure of Anopheles albimanus was studied in southern Central America using partial sequences of the mtDNA cytochrome oxidase subunit I gene (COI). Analysis of molecular variance supported significant genetic structure between populations from Costa Rica and western Panama versus those from central-eastern Panama (ΦCT = 0.33), whereas the within group divergence was shallow and statistically insignificant (ΦST = 0.08). Furthermore, a statistical parsimony network depicted three divergent groups of haplotypes that were not evenly distributed across the study area. Our findings are in partial agreement with previous studies, yet they do not support physical barriers to gene flow or contemporary isolation by distance in this region. Instead, three co-occurring groups of An. albimanus may be the result of multiple introductions, most likely caused by historical fragmentation and subsequent secondary contact. In addition, the molecular signature of population expansion of An. albimanus was detected in central-eastern Panama approximately 22,000 years ago (95% confidence interval [CI] 10,183–38,169). We hypothesize that the population structure of An. albimanus, as determined by our COI locus analysis, is the result of late Pleistocene climatic changes in northern South America.
Financial support: The Secretariat for Science, Technology and Innovation of Panama (SENACYT) through a scholarship and research grant COL08-066 awarded to Jose Loaiza, partially financed this research. Additional financial support was provided by the Smithsonian Tropical Research Institute (STRI), the Organization of American States (OAS), Natural Sciences and Engineering Research Council of Canada (NSERC), and National Institutes of Health (NIH) grant (AI) R0154139-02 to JEC. Research at the Institute of Parasitology is supported by a regroupement stratégique from Fonds Québécois de la recherche sur la nature et les technologies (FQRNT).
Authors' addresses: Jose R. Loaiza and Marilyn E. Scott, Department of Natural Resource Sciences, McGill University, Ste. Anne de Bellevue, Quebec, Canada, E-mails: jose.loaiza@mail.mcgill.ca and marilyn.scott@mcgill.ca. Eldredge Bermingham, Smithsonian Tropical Research Institute, Balboa Ancon, Republic of Panama, E-mail: bermingham@si.edu. Jose Rovira, Departamento de Entomologia Medica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Ciudad de Panama, E-mail: jrovira@gorgas.gob.pa. Jan E. Conn, Griffin Laboratory, The Wadsworth Center, New York State Department of Health, Slingerlands, NY, E-mail: jconn@wadsworth.org.
Pan American Health Organization, 2006. Regional Strategic Plan for Malaria in the Americas 2006–2010. Washington, DC: Pan American Health Organization.
Ministerio Nacional de Salud de Panamá, 2007. Análisis de la Situación de Malaria en Panamá. Boletín Epidemiológico. Available at: http://www.minsa.gob.pa. Accessed May 4, 2009.
Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE, 2008. Species composition and distribution of adult Anopheles (Diptera: Culicidae) in Panama. J Med Entomol 45: 841–851.
Calzada EJ, Samudio F, Bayard V, Obaldia N, De Mosca IB, Pascale JM, 2009. Revising antimalarial drug policy in Central America: experience of Panama. Trans R Soc Trop Med Hyg 102: 694–698.
Loaiza J, Scott M, Bermingham E, Rovira J, Conn J, 2009. Short report: Anopheles darlingi in Panama. Am J Trop Med Hyg 81: 23–26.
Lehmann T, Licht M, Elissa N, Maega BT, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA, 2003. Population structure of Anopheles gambiae in Africa. J Hered 94: 133–147.
Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Povoa MM, Padilla N, Nicole LA, Conn JE, 2008. Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol 8: 3.
Walton C, Handley JM, Tun-Lin W, 2000. Population structure and population history of Anopheles dirus mosquitoes in Southeast Asia. Mol Biol Evol 17: 962–974.
Mirabello L, 2007. Molecular Population Genetics of the Malaria Vector Anopheles darlingi throughout Central and South America using Mitochondrial, Nuclear and Microsatellites Markers. Ph.D. Thesis. Albany, NY: University at Albany.
O'Loughlin SM, Okabayashi T, Honda M, Kitazoe Y, Kishino H, Somboon P, Sochantha T, Nambanya S, Saikia PK, Dev V, Walton C, 2008. Complex population history of two Anopheles dirus mosquito species in south Asia suggests the influence of Pleistocene climate change rather than human-mediated effects. J Evol Biol 21: 1555–1569.
Faran ME, 1980. Mosquito studies (Diptera: Culicidae) XXXIV. A revision of the Albimanus section of the subgenus Nyssorhynchus of Anopheles, contrib. Am Entomol Inst 15: 1–215.
Breeland SG, 1972. Studies on the ecology of Anopheles albimanus. Am J Trop Med Hyg 21: 751–754.
Hobbs J, Sexton J, St. Jean Y, Jacques J, 1986. The biting and resting behavior of Anopheles albimanus in northern Haiti. J Am Mosq Control Assoc 2: 150–153.
Beach RF, Mills D, Collins FH, 1989. Structure of ribosomal DNA in Anopheles albimanus (Diptera: Culicidae). Ann Entomol Soc Am 81: 641–648.
Narang SK, Seawright JA, Suarez MF, 1991. Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosq Control Assoc 7: 337–345.
De Merida AM, De Mata MP, Molina E, Porter CH, Black WC, 1995. Variation in ribosomal DNA intergenic spacers among populations of Anopheles albimanus in South and Central America. Am J Trop Med Hyg 53: 469–477.
Collins WE, Skinner JC, Warren M, Richardson B, 1976. Studies on human malaria in Aotus monkeys. VII. Comparative infectivity of two strains of Plasmodium vivax to Anopheles freeborni, An. maculatus, and four strains of An. albimanus. J Parasitol 62: 190–194.
Frederickson EC, 1993. Bionomics and Control of Anopheles albimanus. Washington, DC: Pan American Health Organization, Pan American Sanitary Bureau Regional Office of the World Health Organization.
Grieco JP, Achee NL, Roberts DR, Andre RG, 2005. Comparative susceptibility of three species of Anopheles from Belize, Central America, to Plasmodium falciparum (Nf-54). J Am Mosq Control Assoc 21: 279–290.
Achee NA, Achee N, Grieco JP, Andre RG, Rejmankova E, Roberts DR, 2007. A mark release-recapture study to define the flight behaviours of Anopheles vestitipennis and An. albimanus in Belize, Central America. J Am Mosq Control Assoc 3: 276–282.
De Merida AM, Palmieri M, Yurrita M, Molina A, Molina E, Black WC, 1999. Mitochondrial DNA variation among Anopheles albimanus populations. Am J Trop Med Hyg 6: 230–239.
Molina-Cruz A, De Merida AM, Mills K, Rodriguez F, Schoua C, Yurrita MM, Molina E, Palmieri M, William CB, 2004. Gene flow among Anopheles albimanus populations in Central America, South America, and the Caribbean assessed by microsatellites and mitochondrial DNA. Am J Trop Med Hyg 71: 350–359.
Conn JE, Mirabello L, 2007. The biogeography and population genetics of neotropical vector species. Heredity 99: 245–256.
Fairley TL, Renaud TM, Conn JE, 2000. Effects of local geographic barriers and latitude on population structure in Anopheles punctipennis (Diptera: Culicidae). J Med Entomol 37: 754–760.
Mirabello L, Conn JE, 2006. Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity 96: 311–321.
Wilkerson RC, Strickman D, 1990. Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J Am Mosq Control Assoc 6: 7–34.
Lunt DH, Zhang DX, Szymura JM, Hewitt GM, 1996. The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5: 153–165.
Swofford DL, 2003. PAUP (Phylogenetic Analysis Using Parsimony) and Other Methods, Version 4. Sunderland, MA: Sinauer Associates.
Maddison WP, Maddison DR, 1997. MacClade: Analysis of Phylogeny and Character Evolution, Version 3.07. Sunderland, MA: Sinauer Associates.
Tamura K, Dudley J, Nei M, Kumar S, 2007. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
Clement M, Posada D, Crandall KA, 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657–1659.
Posada D, Crandall KA, Templeton AR, 2000. GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9: 487–488.
Crandall KA, Templeton AR, 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134: 959–969.
Uthicke S, Benzie JAH, 2003. Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holoturoidea) populations from the Indo-Pacific. Mol Ecol 12: 2635–2648.
Excoffier L, Laval G, Schmeider S, 2005. Arlequin (version 3.0): an integrated software package for population genetic data analysis. Evol Bioinform Online 1: 47–50.
Mantel N, 1967. The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209–220.
Jensen J, Bohonak AJ, Kelley ST, 2005. Isolation by distance, web service. BMC Genet 6: 13.
Tajima F, 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics 123: 585–595.
Fu YX, Li WH, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.
Fu YX, 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.
Ramos-Onsins SE, Rozas J, 2002. Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092–2100.
Kimura M, 1983. The Neutral Theory of Molecular Evolution. Cambridge, England: Cambridge University Press.
Rozas J, Sanchez-Del Rio JC, Messeguer X, Rozas R, 2003. DnaSP, DNA polymorphism analyses by the coalescence and other methods. Bioinformatics 19: 2496–2497.
Nei M, 1987. Molecular Evolutionary Genetics. New York: Columbia University Press.
Harpending HC, Sherry ST, Rogers AR, Stoneking M, 1993. The genetic structure of ancient human populations. Curr Anthropol 34: 483–496.
Rogers AR, 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49: 608–615.
Tamura K, Nei M, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512–526.
Castelloe J, Templeton AR, 1994. Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phyl Evol 3: 102–113.
Powell JR, Caccone A, Amato GD, Yoon C, 1986. Rate of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83: 9090–9093.
Mirabello L, Conn JE, 2008. Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol 22: 109–119.
Conn JE, Vineis JH, Bollback JP, Onyabe DY, Wilkerson RC, Póvoa MM, 2006. Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg 74: 798–806.
Scarpassa VM, Conn JE, 2007. Population genetic structure of the major malaria vector Anopheles darlingi (Diptera: Culicidae) from the Brazilian Amazon, using microsatellite markers. Mem Inst Oswaldo Cruz 102: 319–327.
Conn J, Mitchell SE, Cockburn AF, 1998. Mitochondrial DNA analysis of the neotropical malaria vector Anopheles nuneztovari. Genome 41: 313–327.
Telles MP, Diniz-Filho JA, 2005. Multiple Mantel test and isolation by distance, taking into account long-term historical divergence. Genet Mol Res 4: 742–748.
Trapido H, 1952. Modified response of Anopheles albimanus to DDT residual house spraying in Panama. Am J Trop Med Hyg 15: 853–861.
Zink RM, Barrowclough GF, 2008. Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17: 2107–2121.
Templeton AR, 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7: 381–397.
Kolbe JJ, Glor RE, Schettino LR, Lara AD, Larson A, Losos JB, 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177–181.
Gonzáles C, Urrego LE, Martínez JI, 2006. Late quaternary vegetation and climate change in the Panama basin: palynological evidence from marine cores ODP 677 and TR 163-38. PALAEO 234: 62–80.
Golik A, 1968. History of the Holocene transgression in the Gulf of Panama. J Geol 76: 497–507.
Bermingham E, Martin AP, 1998. Comparative mtDNA phylogeography of neotropical fresh water fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol 7: 499–517.
Zeh JA, Zeh DW, Bonilla MM, 2003. Phylogeography of the harlequin beetle-riding pseudoscorpion and the rise of the Isthmus of Panama. Mol Ecol 12: 2759–2769.
Weigt LA, Crawford AJ, Stanley Rand A, Ryan M, 2005. Biogeography of the tungara frog, Physalaemus pustulosus: a molecular perspective. Mol Ecol 14: 3857–3876.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 299 | 228 | 21 |
Full Text Views | 565 | 12 | 4 |
PDF Downloads | 124 | 19 | 4 |