Phylogenetic and phylogeographic insights on Trans-Andean spectacled caiman populations in Colombia
Gonzalo Jiménez-Alonso
A B * , Sergio A. Balaguera-Reina C , Manuel Hoyos A , Carolina Ibáñez A , Sandra Marcela Hernández Rangel A , Carlos Miguel del Valle Useche A , Juan Felipe Moncada D and Paul Bloor A
+ Author Affiliations
- Author Affiliations
A Grupo Biodiversidad y Conservación Genética, Instituto de Genética, Universidad Nacional de Colombia, Bogotá, DC, Colombia.
B Programa de Zootecnia, Facultad de Ciencias Agrarias, Fundación Universitaria Agraria de Colombia-UNIAGRARIA, Calle 170 #54ª-10, Bogotá, DC 111166, Colombia.
C Fort Lauderdale Research and Education Center, University of Florida, Davie, FL 33314, USA.
D Programa de Biología, Facultad de Ciencias, Universidad de Tolima, Calle 42 #1B-1 Barrio Santa Helena, Ibagué 730001, Colombia.
Marine and Freshwater Research 74(12) 1071-1080 https://doi.org/10.1071/MF22251
Submitted: 22 November 2022 Accepted: 7 June 2023 Published: 30 June 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Spectacled caiman (Caiman crocodilus) is a species complex with at least eight phylogenetic lineages distributed across Central and South America. However, several populations remain unstudied, which limits a clear understanding of the relationship among lineages as well as whether all hidden diversity has been unveiled.
Aim: We analysed the molecular variation of spectacled caiman populations inhabiting the Colombian Trans-Andean range based on cytochrome oxidase I (COI) and cytochrome B (CytB) mitochondrial markers.
Methods: We performed phylogenetic and population genetic analysis to identify phylogeographic patterns and verify genetic variation across Trans-Andean spectacled caiman by using a dataset of 78 individuals from 15 localities across Colombia.
Results: Haplotype accumulation curve estimated that our sample sizes recovered 82.68% of all unique haplotypes. Analysis of molecular variance showed that most of the genetic variation across the Trans-Andean samples collected can be explained by macro basins (49.85%), 32.45% by localities and 17.70% by intra-specific variation within populations.
Conclusions: Our study confirmed that high nucleotide diversity is present in Colombian Trans-Andean spectacled caiman populations, the absence of a genetically distinguished lineage in the Choco region, as suggested by morphologic analysis, and the presence of only one molecularly well distinguished group (C. c. fuscus sensu stricto) in the in the Colombian Trans-Andean region.
Keywords: Caribbean region, conservation, crocodylians, evolutionary history, management, mitochondrial DNA, Pacific region, reptiles.
References
Alacs, EA, Georges, A, FitzSimmons, NN, and Robertson, J (2010). DNA detective: a review of molecular approaches to wildlife forensics. Forensic Science, Medicine, and Pathology 6, 180–194.| DNA detective: a review of molecular approaches to wildlife forensics.Crossref | GoogleScholarGoogle Scholar |
Albert JS, Reis RE (2011) Introduction to neotropical freshwaters. In ‘Historical biogeography of neotropical freshwater fishes’. (Eds JS Albert, RE Reis) pp. 3–18. (University of California Press: Berkeley, CA, USA)
Albert, JS, Lovejoy, NR, and Crampton, WGR (2006). Miocene tectonism and the separation of cis- and trans-Andean river basins: evidence from Neotropical fishes. Journal of South American Earth Sciences 21, 14–27.
| Miocene tectonism and the separation of cis- and trans-Andean river basins: evidence from Neotropical fishes.Crossref | GoogleScholarGoogle Scholar |
Altschul, SF, Gish, W, Miller, W, Myers, EW, and Lipman, DJ (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
| Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar |
Angulo-Bedoya, M, Correa, S, and Benítez, HA (2019). Unveiling the cryptic morphology and ontogeny of the Colombian Caiman crocodilus: a geometric morphometric approach. Zoomorphology 138, 387–397.
| Unveiling the cryptic morphology and ontogeny of the Colombian Caiman crocodilus: a geometric morphometric approach.Crossref | GoogleScholarGoogle Scholar |
Avise, JC, Arnold, J, Ball, RM, Bermingham, E, Lamb, T, Neigel, JE, Reeb, CA, and Saunders, NC (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18, 489–522.
| Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics.Crossref | GoogleScholarGoogle Scholar |
Balaguera-Reina, SA, and Densmore, LD (2014). Legislation and conservation efforts concerning crocodiles in Colombia: a historical review. Herpetological Review 45, 638–642.
Balaguera-Reina SA, Velasco A (2019) Spectacled Caiman Caiman crocodilus. In ‘The IUCN Red List of Threatened Species 2019’. e.T46584A3009688. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/46584/3009688
Balaguera-Reina, SA, Moncada-Jimenez, JF, Prada-Quiroga, CF, Hernandez-Gonzalez, F, Bolaños-Cubillos, NW, Farfán-Ardila, N, Garcia-Calderón, LM, and Densmore, LD (2020a). Tracking a voyager: mitochondrial DNA analyses reveal mainland-to-island dispersal of an American crocodile (Crocodylus acutus) across the Caribbean. Biological Journal of the Linnean Society 131, 647–655.
| Tracking a voyager: mitochondrial DNA analyses reveal mainland-to-island dispersal of an American crocodile (Crocodylus acutus) across the Caribbean.Crossref | GoogleScholarGoogle Scholar |
Balaguera-Reina, SA, Vargas-Ramírez, M, Ordóñez-Garza, N, Hernández-González, F, and Densmore, LD (2020b). Unveiling the mystery: assessing the evolutionary trajectory of the Apaporis caiman population (Caiman crocodilus apaporiensis, Medem 1955) via mitochondrial molecular makers. Biological Journal of the Linnean Society 131, 163–171.
| Unveiling the mystery: assessing the evolutionary trajectory of the Apaporis caiman population (Caiman crocodilus apaporiensis, Medem 1955) via mitochondrial molecular makers.Crossref | GoogleScholarGoogle Scholar |
Balaguera-Reina, SA, Konvalina, JD, Mohammed, RS, Gross, B, Vazquez, R, Moncada, JF, and Densmore, LD (2021). From the river to the ocean: mitochondrial DNA analyses provide evidence of spectacled caimans (Caiman crocodilus Linnaeus 1758) mainland–insular dispersal. Biological Journal of the Linnean Society 134, 486–497.
| From the river to the ocean: mitochondrial DNA analyses provide evidence of spectacled caimans (Caiman crocodilus Linnaeus 1758) mainland–insular dispersal.Crossref | GoogleScholarGoogle Scholar |
Balaguera-Reina, SA, Angulo-Bedoya, M, Moncada-Jimenez, JF, Webster, M, Roberto, IJ, and Mazzotti, FJ (2022). Update: assessing the evolutionary trajectory of the Apaporis caiman (Caiman crocodilus apaporiensis, Medem 1955) via mitochondrial molecular markers. Biological Journal of the Linnean Society 137, 700–710.
| Update: assessing the evolutionary trajectory of the Apaporis caiman (Caiman crocodilus apaporiensis, Medem 1955) via mitochondrial molecular markers.Crossref | GoogleScholarGoogle Scholar |
Bermingham, E, and Moritz, C (1998). Comparative phylogeography: concepts and applications. Molecular Ecology 7, 367–369.
| Comparative phylogeography: concepts and applications.Crossref | GoogleScholarGoogle Scholar |
Bittencourt, PS, Campos, Z, Muniz, FdL, Marioni, B, Souza, BC, Da Silveira, R, de Thoisy, B, Hrbek, T, and Farias, IP (2019). Evidence of cryptic lineages within a small South American crocodilian: the Schneider’s dwarf caiman Paleosuchus trigonatus (Alligatoridae: Caimaninae). PeerJ 7, e6580.
| Evidence of cryptic lineages within a small South American crocodilian: the Schneider’s dwarf caiman Paleosuchus trigonatus (Alligatoridae: Caimaninae).Crossref | GoogleScholarGoogle Scholar |
Brochu, CA (1999). Phylogeny, systematics, and historical biogeography of Alligatoroidea. Society of Vertebrate Paleontology Memoir 6, 9–100.
Cadle, JE (1985). The neotropical colubrid snake fauna (Serpentes: Colubridae): lineage components and biogeography. Systematic Zoology 34, 1–20.
| The neotropical colubrid snake fauna (Serpentes: Colubridae): lineage components and biogeography.Crossref | GoogleScholarGoogle Scholar |
Chessel, D, Dufour, AB, and Thioulouse, J (2004). The ade4 package. I. One-table methods. R News 4, 5–10.
Clement, M, Posada, D, and Crandall, KA (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar |
da Silva, MNF, and Patton, JL (1998). Molecular phylogeography and the evolution and conservation of Amazonian mammals. Molecular Ecology 7, 475–486.
| Molecular phylogeography and the evolution and conservation of Amazonian mammals.Crossref | GoogleScholarGoogle Scholar |
De la Ossa-Guerra, LE, Santos, MH, and Artoni, RF (2020). Genetic diversity of the cichlid Andinoacara latifrons (Steindachner, 1878) as a conservation strategy in different Colombian Basins. Frontiers in Genetics 11, 815.
| Genetic diversity of the cichlid Andinoacara latifrons (Steindachner, 1878) as a conservation strategy in different Colombian Basins.Crossref | GoogleScholarGoogle Scholar |
Duellman WE (1999) Distribution patterns of amphibians in South America. In ‘Patterns of distribution of amphibians: a global perspective’. (Ed. WE Duellman) pp. 255–328. (Johns Hopkins University Press: Baltimore, MD, USA)
Díaz-Moreno, DM, Hernández-Gonzalez, F, Moncada-Jimenez, JF, Mora, C, Prada, C, Jiménez-Alonso, G, and Balaguera-Reina, SA (2021). Molecular characterization of the spectacled caiman (Caiman crocodilus) in the upper Magdalena River Basin, Colombia: demographic and phylogeographic insights. Systematics and Biodiversity 19, 1040–1048.
| Molecular characterization of the spectacled caiman (Caiman crocodilus) in the upper Magdalena River Basin, Colombia: demographic and phylogeographic insights.Crossref | GoogleScholarGoogle Scholar |
Edgar, RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar |
Escobedo-Galván, AH, Velasco, J, Gonzalez-Maya, JF, and Resetar, A (2015). Morphometric analysis of the Rio Apaporis Caiman (Reptilia, Crocodylia, Alligatoridae). Zootaxa 4059, 541–554.
| Morphometric analysis of the Rio Apaporis Caiman (Reptilia, Crocodylia, Alligatoridae).Crossref | GoogleScholarGoogle Scholar |
Excoffier, L, and Lischer, HEL (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |
Farias, IP, Da Silveira, R, de Thoisy, B, Monjeló, LA, Thorbjarnarson, J, and Hrbek, T (2004). Genetic diversity and population structure of Amazonian crocodilians. Animal Conservation 7, 265–272.
| Genetic diversity and population structure of Amazonian crocodilians.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (2004) ‘Inferring phylogenies. Vol. 2.’ (Sinauer Associates: Sunderland, MA, USA)
Guindon, S, Dufayard, J-F, Lefort, V, Anisimova, M, Hordijk, W, and Gascuel, O (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar |
Halas, D, Zamparo, D, and Brooks, DR (2005). A historical biogeographical protocol for studying biotic diversification by taxon pulses. Journal of Biogeography 32, 249–260.
| A historical biogeographical protocol for studying biotic diversification by taxon pulses.Crossref | GoogleScholarGoogle Scholar |
Hallas, JM, Parchman, TL, and Feldman, CR (2021). The influence of history, geography and environment on patterns of diversification in the western terrestrial garter snake. Journal of Biogeography 48, 2226–2245.
| The influence of history, geography and environment on patterns of diversification in the western terrestrial garter snake.Crossref | GoogleScholarGoogle Scholar |
Hurvich, CM, and Tsai, C-L (1993). A corrected Akaike information criterion for vector autoregressive model selection. Journal of Time Series Analysis 14, 271–279.
| A corrected Akaike information criterion for vector autoregressive model selection.Crossref | GoogleScholarGoogle Scholar |
Instituto de Hidrologia, Meteorologia y Estudios Ambientales (2013) ‘Zonificación y codificación de unidades hidrográficas e hidrológicas de Colombia.’ [‘Zoning and codification of hydrographic and hydrological units of Colombia.’] (Imprenta Nacional de Colombia: Bogota, Colombia) [In Spanish]
Iturralde-Vinent, MA (2006). Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region. International Geology Review 48, 791–827.
| Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region.Crossref | GoogleScholarGoogle Scholar |
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, and Drummond, A (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |
King FW, Burke RL (1989) ‘Crocodilian, tuatara, and turtle species of the world. A taxonomic and geographic reference.’ (Association of Systematics Collections: Washington, DC, USA)
Lanfear, R, Calcott, B, Ho, SYW, and Guindon, S (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T, and Calcott, B (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Lanteri AA, Confalonieri VA (2003) Filogeografía: objetivos, métodos y ejemplos. In ‘Una perspectiva latinoamericana de la biogeografía’. (Eds JJ Morrone, J Llorente) pp. 185–194. (UNAM)
Leigh, JW, and Bryant, D (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.
| POPART: full-feature software for haplotype network construction.Crossref | GoogleScholarGoogle Scholar |
Marshall, CJ, and Liebherr, JK (2000). Cladistic biogeography of the Mexican transition zone. Journal of Biogeography 27, 203–216.
| Cladistic biogeography of the Mexican transition zone.Crossref | GoogleScholarGoogle Scholar |
Medem F (1981) ‘Los Crocodylia de Sur América: Los Crocodylia de Colombia. Vol. 1.’ [‘South American Crocodylians: Crocodylians from Colombia.’] (Colciencias: Bogotá, Colombia) [In Spanish]
Mullis K, Faloona F, Scharf S, Saiki R, Horn G, Erlich H (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harbor Symposia on Quantitative Biology 51, 263–273. 10.1101/SQB.1986.051.01.032
Muniz, FL, Campos, Z, Hernández Rangel, SM, Martínez, JG, Souza, BC, De Thoisy, B, Botero-Arias, R, Hrbek, T, and Farias, IP (2018). Delimitation of evolutionary units in Cuvier’s dwarf caiman, Paleosuchus palpebrosus (Cuvier, 1807): insights from conservation of a broadly distributed species. Conservation Genetics 19, 599–610.
| Delimitation of evolutionary units in Cuvier’s dwarf caiman, Paleosuchus palpebrosus (Cuvier, 1807): insights from conservation of a broadly distributed species.Crossref | GoogleScholarGoogle Scholar |
Muniz, FL, Ximenes, AM, Bittencourt, PS, Hernández-Rangel, SM, Campos, Z, Hrbek, T, and Farias, IP (2019). Detecting population structure of Paleosuchus trigonatus (Alligatoridae: Caimaninae) through microsatellites markers developed by next generation sequencing. Molecular Biology Reports 46, 2473–2484.
| Detecting population structure of Paleosuchus trigonatus (Alligatoridae: Caimaninae) through microsatellites markers developed by next generation sequencing.Crossref | GoogleScholarGoogle Scholar |
Nei M, Kumar S (2000) ‘Molecular evolution and phylogenetics.’ (Oxford University Press)
Ogden, R, and Linacre, A (2015). Wildlife forensic science: a review of genetic geographic origin assignment. Forensic Science International: Genetics 18, 152–159.
| Wildlife forensic science: a review of genetic geographic origin assignment.Crossref | GoogleScholarGoogle Scholar |
Parra-Olea, G, García-París, M, and Wake, DB (2004). Molecular diversification of salamanders of the tropical American genus Bolitoglossa (Caudata: Plethodontidae) and its evolutionary and biogeographical implications. Biological Journal of the Linnean Society 81, 325–346.
| Molecular diversification of salamanders of the tropical American genus Bolitoglossa (Caudata: Plethodontidae) and its evolutionary and biogeographical implications.Crossref | GoogleScholarGoogle Scholar |
Patwardhan, A, Ray, S, and Roy, A (2014). Molecular markers in phylogenetic studies – a review. Journal of Phylogenetics & Evolutionary Biology 2, 131.
| Molecular markers in phylogenetic studies – a review.Crossref | GoogleScholarGoogle Scholar |
Phillips, JD, French, SH, Hanner, RH, and Gillis, DJ (2020). HACSim: an R package to estimate intraspecific sample sizes for genetic diversity assessment using haplotype accumulation curves. PeerJ Computer Science 6, e243.
| HACSim: an R package to estimate intraspecific sample sizes for genetic diversity assessment using haplotype accumulation curves.Crossref | GoogleScholarGoogle Scholar |
Rincon-Sandoval, M, Betancur-R, R, and Maldonado-Ocampo, JA (2019). Comparative phylogeography of trans-Andean freshwater fishes based on genome-wide nuclear and mitochondrial markers. Molecular Ecology 28, 1096–1115.
| Comparative phylogeography of trans-Andean freshwater fishes based on genome-wide nuclear and mitochondrial markers.Crossref | GoogleScholarGoogle Scholar |
Roberto, IJ, Bittencourt, PS, Muniz, FL, Hernández-Rangel, SM, Nóbrega, YC, Ávila, RW, Souza, BC, Alvarez, G, Miranda-Chumacero, G, Campos, Z, Farias, IP, and Hrbek, T (2020). Unexpected but unsurprising lineage diversity within the most widespread Neotropical crocodilian genus Caiman (Crocodylia, Alligatoridae). Systematics and Biodiversity 18, 377–395.
| Unexpected but unsurprising lineage diversity within the most widespread Neotropical crocodilian genus Caiman (Crocodylia, Alligatoridae).Crossref | GoogleScholarGoogle Scholar |
Rohland, N, and Hofreiter, M (2007). Comparison and optimization of ancient DNA extraction. BioTechniques 42, 343–352.
| Comparison and optimization of ancient DNA extraction.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA, and Huelsenbeck, JP (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. In ‘Bioinformatics for DNA sequence analysis. Methods in Molecular Biology. Vol. 537’. (Ed. D Posada) pp. 337–350. (Humana Press)
Sanger, F, and Coulson, AR (1975). A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. Journal of Molecular Biology 94, 441–448.
| A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase.Crossref | GoogleScholarGoogle Scholar |
Savage, JM (1982). The enigma of the Central American herpetofauna: dispersals or vicariance. Annals of the Missouri Botanical Garden 69, 464–547.
| The enigma of the Central American herpetofauna: dispersals or vicariance.Crossref | GoogleScholarGoogle Scholar |
Savage, JM (1987). Systematics and distribution of the Mexican and Central American rainfrogs of the Eleutherodactylus gollmeri group (Amphibia: Leptodactylidae). Fieldiana Zoology 33, 1–57.
Schneider, CJ, Cunningham, M, and Moritz, C (1998). Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia. Molecular Ecology 7, 487–498.
| Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia.Crossref | GoogleScholarGoogle Scholar |
Tamura, K, and 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.
| Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Crossref | GoogleScholarGoogle Scholar |
Vasconcelos, WR, Hrbek, T, Silveira, R, Thoisy, B, Marioni, B, and Farias, IP (2006). Population genetic analysis of Caiman crocodilus (Linnaeus, 1758) from South America. Genetics and Molecular Biology 29, 220–230.
| Population genetic analysis of Caiman crocodilus (Linnaeus, 1758) from South America.Crossref | GoogleScholarGoogle Scholar |
Venegas-Anaya, M, Crawford, AJ, Galván-Escobedo, AH, Sanjur, OI, Densmore, LD, and Bermingham, E (2008). Mitochondrial DNA phylogeography of Caiman crocodilus in Mesoamerica and South America. Journal of Experimental Zoology – A. Ecological Genetics and Physiology 309A, 614–627.
| Mitochondrial DNA phylogeography of Caiman crocodilus in Mesoamerica and South America.Crossref | GoogleScholarGoogle Scholar |
