Evidence of hybridization in the Argentinean lizards Liolaemus gracilis and Liolaemus bibronii (IGUANIA: LIOLAEMINI): An integrative approach based on genes and morphology

Molecular Phylogenetics and Evolution

Volumn 61, Issue 2, 2011, Pages 381-391

  Olave, Melisa ^a   Martinez, Lorena E ^a   Avila, Luciano J ^a   Sites, Jack W ^b   Morando, Mariana ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Introngression; Liolaemini; MtDNA; Nuclear DNA; Patagonia; Phylogeography

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARGENTINA; ARTICLE; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; FEMALE; GENETICS; HAPLOTYPE; HISTOLOGY; HYBRIDIZATION; LIZARD; MALE; PHYLOGENY; POPULATION GENETICS; SYMPATRY;

ANIMALS; ARGENTINA; CELL NUCLEUS; DNA, MITOCHONDRIAL; FEMALE; GENETICS, POPULATION; HAPLOTYPES; HYBRIDIZATION, GENETIC; LIZARDS; MALE; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SYMPATRY;

IGUANIA; LIOLAEMUS; LIOLAEMUS BIBRONII; LIOLAEMUS GRACILIS; SQUAMATA;

EID: 80052722268     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.07.006     Document Type: Article

References (100)

1. Abdala C.S. Cuatro nuevas especies del genero Liolaemus (Iguania: Liolaemidae), pertenecientes al grupo boulengeri, de la Patagonia. Argentina. Cuadernos de Herpetología 2003, 17:3-32.
2. Abdala C.S. Dos nuevas especies del género Liolaemus (Iguania: Liolaemidae) y redescripción de Liolaemus boulengeri (Koslowky, 1898). Cuadernos de Herpetología 2005, 19:3-33.
3. Andersson M. Sexual Selection 1994, Princeton University Press, New Jersey.
4. Arnold M.L. Natural Hybridization and Evolution 1997, Oxford University Press, New York.
5. Avila L.J., Cei J.M., Martori R.A., Acosta J.C. A new species of Liolaemus of the bibroni group from granitic ravines of Achiras, Sierra de Comechingones, Córdoba, Argentina (Reptilia: Tropiduridae). Museo Regionale di Scienze Natural Turín 1992, 10:101-111.
6. Avila L.J., Perez C.H.F., Morando M. A new species of Liolaemus (Squamata: Iguania: Liolaemidae) from northwestern Patagonia (Neuquen, Argentina). Herpetologica 2003, 59:532-543.
7. Avila L.J., Morando M., Sites J.W. Congeneric phylogeography: hypothesizing species limits and evolutionary processes in Patagonian lizards of the Liolaemus boulengeri group (Squamata: Liolaemini). Biological Journal of the Linnaean Society 2006, 89:241-275.
8. Avila L.J., Morando M., Perez D.R., Sites J.W. A new species of the Liolaemus elongatus clade (Reptilia: Iguania: Liolaemini) from Cordillera del Viento, northwestern Patagonia, Neuquén, Argentina. Zootaxa 2010, 2667:28-42.
9. Avise J.C., Ball R.M. Principles of genealogical concordance in species concepts and biological taxonomy. Surveys in Evolutionary Biology 1990, vol. 7:45-67. Oxford University Press.
10. Barbujani G.A., Pilastro A., Dedomenico S., Renfrew C. Genetic variation in North Africa and Eurasia-Neolithic demic diffusion verses Palaeolithic colonization. American Journal of Physical Anthropology 1994, 95:137-154.
11. Belfiore N.M., Liu L., Moritz C. Multilocus phylogenetics of a rapid radiation in the genus Thomomys (Rodentia: Geomyidae). Systematic Biology 2008, 57:294-310. 10.1080/10635150802044011.
12. Bell M.A., Travis M.P. Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends in Ecology & Evolution 2005, 20:358-361.
13. Bossu C.M., Near T.J. Gene trees reveal repeated instances of mitochondrial DNA introgression in orangethroat darters (Percidae: Etheostoma). Systematic Biology 2009, 58:114-129.
14. Brumfield R.T., Liu L., Lum D.E., Edwards S.V. Comparison of species tree methods for reconstructing the phylogeny of bearded manakins (Aves: Pipridae: Manacus) from multilocus sequence data. Systematic Biology 2008, 57:719-731.
15. Carling M.D., Brumfield R.T. Integrating phylogenetic and population genetic analyses of multiple loci to test species divergence hypotheses in Passerina buntings. Genetics 2008, 178:363-377. 10.1534/genetics.107.076422.
16. Carothers J.H. Sexual selection and sexual dimorphism in some herbivorous lizards. American Naturalist 1984, 124:244-254.
17. Carpenter C.C., Ferguson G.W. Variation and evolution of stereotyped behavior in reptiles. Biology of the Reptilia. Ecology and Behavior A 1977, vol. 7:335-554. Academic Press, London.
18. Cei J.M. Reptiles del centro, centro-oeste y sur de la Argentina. **Museo. Regionale di Scienze Naturali. Torino, Monografía 1986, 4:1-527.
19. Cei, J.M., 1993. Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, Puna y Pampas. Museo Regionale di Scienze Naturali. Torino, Monografía XIV, 949 pp.
20. Cei J.M., Scolaro J.A. Speciation of the ''darwinii complex'' (genus Liolaemus, ''patch group'') in the southern-most area of its distribution (Reptilia: Tropiduridae). **Rev. Fr. Aquariol. 1999, 26:79-82.
21. Chan K.M.A., Levin S.A. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 2005, 59:720-729.
22. Chiba S. Appearance of morphological novelty in a hybrid zone between two species of land snail. Evolution 2005, 59:1712-1720.
23. Clapperton C.M. Quaternary Geology and Geomorphology of South America 1993, Elsevier, Amsterdam.
24. Degnan J.H., Rosenberg N.A. Gene tree discordance, phylogenetic inference, and the multispecies coalescent. Trends in Ecology & Evolution 2009, 24:332-340.
25. Donoso-Barros R. Reptiles de Chile 1966, Ediciones de la Universidad de Chile, Santiago, Chile.
26. Drummond, A.J., Rambaut, A., 2006. BEAST v1.4. http://beast.bio.edsac.uk/.
27. Eckert A.J., Carstens B.C. Does gene flow destroy phylogenetic signal? The performance of three methods for estimating phylogenies in the presence of gene flow. Molecular Phylogenetics and Evolution 2008, 49:832-842.
28. Edwards S., Bensch S. Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Molecular Ecology 2009, 18:2930-2933.
29. Etheridge R. A new psammophilus lizard of the genus Liolaemus (Squamata: Tropiduridae) from northwestern Argentina. Museo Regionale di Scienze Natural 1992, 10:1-19.
30. Etheridge R. Lizards of the Liolaemus darwinii complex (Squamata: Iguania: Tropiduridae) in northern Argentina. Museo Regionale di Scienze Natural 1993, 119:137-199.
31. Etheridge R. Redescription of Ctenoblepharys adspersa (Tschudi, 1845), and the taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae). American Museum Novitates 1995, 3142:1-34.
32. Etheridge R. A new species of Liolaemus (Reptilia: Squamata: Liolaemidae) from Mendoza Province. Argentina. Cuadernos de Herpetología 2001, 15:3-15.
33. Etheridge R., Christie M.L. Two new species of the lizard genus Liolaemus (Squamata: Liolaemidae) from northern Patagonia, with comments on Liolaemus rothi. Journal of Herpetology 2003, 37:325-341.
34. Etheridge, R., De Queiroz, K., 1988. A phylogeny of Iguanidae. Edición R. Estes & G. Pregill. pp. 283-368.
35. Fairbairn D.J. Allometry for sexual size dimor- phism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 1997, 28:659-687.
36. Ferris S.D., Sage R.D., Huang C.M., Nielsen J.T., Ritte U., Wilson A.C. Flow of mitochondrial DNA across a species boundary. Proceedings of the National Academy of Sciences of the United States of America 1983, 80:2290-2294.
37. Fu Y.X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
38. Funk D.J., Omland K.E. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics 2003, 34:397-423.
39. Goodman S.J., Barton N.H., Swanson G., Abernethy K., Pemberton J.M. Introgression through rare hybridisation: a genetic study of a hybrid zone between red and sika deer (genus Cervus), in Argyll, Scotland. Genetics 1999, 152:355-371.
40. Guindon S., Gascuel O. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 2003, 52:696-704.
41. Harrison R. Molecular changes at speciation. Annual Review of Ecology and Systematics 1991, 22:281-308.
42. Heath L., Van der Walt E., Varsani A., Martin D.P. Recombination patterns in aphthoviruses mirror those found in other picornaviruses. Journal of Virology 2006, 80:11827-11832.
43. Hedrick A.V., Temeles E.J. The evolution of sexual dimorphism in animals: hypotheses and tests. Trends in Ecology & Evolution 1989, 4:136-138.
44. Heisig M. An etho-ecological study of an island population of Tropidurus atacamensis. Salamandra 1993, 29:65-81.
45. Hellmich W. Über eine neue Liolaemus-Art aus den Bergen von Catamarca, Argentinien. Senckenbergiana Biologica 1964, 45:505-507.
46. Higgins D.G., Sharp P.M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 1988, 73:237-244.
47. Hudson R.R. Gene trees, species trees and the segregation of ancestral alleles. Genetics 1992, 131:509-512.
48. Huelsenbeck J.P., Ronquist F. MRBAYES: bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
49. Knowles L.L. Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology 2001, 10:691-701.
50. Knowles L.L. Statistical phylogeography. Annual Review of Ecology and Systematics 2009, 40:593-612.
51. Knowles L.L., Carstens B.C. Estimating a geographically explicit model of population divergence. Evolution 2007, 61:477-493.
52. Leaché A.D. Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Systematic Biology 2009, 58:547-559.
53. Leaché A.D., Cole C.J. Hybridization between multiple fence lizard lineages in an ecotone: locally discordant variation in mitochondrial DNA, chromosomes, and morphology. Molecular Ecology 2007, 16:1035-1054.
54. Leaché A.D., McGuire J.A. Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: Evidence for amisleading mitochondrial gene tree. Molecular Phylogenetics and Evolution 2006, 39:628-644.
55. Lobo F. A phylogenetic analysis of lizards of the Liolaemus chilensis group (Iguania: Tropiduridae). Herpetological Journal 2001, 11:137-150.
56. Lobo F., Espinoza R.E. Two new cryptic species of Liolaemus (Iguania: Tropiduridae) from nothwestern Argentina: resolution of the purported reproductive biomodality of Liolaemus alticolor. Copeia 1999, 1999:122-140.
57. Lobo F., Kretzschmar S. Descripción de una nueva especie de Liolaemus (Iguania: Tropiduridae) de la Provincia de Tucumán. Neotrópica 1996, 42:33-40.
58. Lobo F., Espinoza R.E., Quinteros S. A critical review and systematic discusión of recent classification proposals for liolaemid lizards. Zootaxa 2010, 2549:1-30.
59. Maddison W. Gene trees in species trees. Systematic Biology 1997, 46:523-536.
60. Manzur M.I., Fuentes E.R. Polygyny and agonistic behavior in the tree-dwelling lizard Liolaemus tenuis (Iguanidae). Behavioral Ecology and Sociobiology 1979, 6:23-28.
61. Marshall J.C., Sites J.W. A comparison of nuclear and mitochondrial cline shapes in a hybrid zone in the Sceloporus grammicus complex (Squamata; Phrynosomatidae). Molecular Ecology 2001, 10:435-449.
62. Martin D., Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
63. McGuire J.A., Linkem C.W., Koo M.S., Hutchison D.W., Lappin A.K., Orange D.I., Lemos-Espinal J.A., Riddle B.R., Jaeger J.R. Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards. Evolution 2007, 61:2879-2897.
64. Moore W. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution: International Journal of Organic Evolution 1995, 49:718-726.
65. Morando M., Avila L.J., Sites J.W. Sampling strategies for delimiting species: genes, individuals and populations in the Liolaemuselongatus-kriegi complex (Squamata: Liolaemimidae) in Andean-Patagonian South America. Systematic Biology 2003, 52:159-185.
66. Morando M., Avila L.J., Baker J.J., Sites J.W. Phylogeny and phylogeography of the Liolaemus darwinii complex (Squamata: Liolaemidae): evidence for introgretion and incomplete lineage sorting. Evolution 2004, 58:842-861.
67. Morando M., Avila L.J., Turner C., Sites J.W. Molecular evidence for species complex in the Patagonian lizard Liolaemus bibronii and phylogeography of the closely related Liolaemus gracilis (Squamata: Liolaemini). Molecular Phylogenetics and Evolution 2007, 43:952-973.
68. Moritz C., Schneider C.J., Wake D.B. Evolutionary relationships within the Ensatina eschscholtzii comples confirm the ring species interpretation. Systematic Biology 1992, 41:273-291.
69. Nei M. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, United States of America 1973, 70:3321-3323.
70. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
71. Nei M. Molecular Evolutionary Genetics 1987, Columbia, New York.
72. Noonan B., Yoder A.D. Anonymous nuclear markers for Malagasy plated lizards (Zonosaurus). Molecular Ecology Resources 2009, 9:402-404.
73. Pamilo P., Nei M. Relationships between gene trees and species trees. Molecular Biology and Evolution 1988, 5:568-583.
74. Pincheira-Donoso D., Scolaro A., Schulte J. The limits of polymorphism in Liolaemus rothi: Molecular and phenotypic evidence for a new species of the Liolaemus boulengeri clade (Iguanidae, Liolaemini) from boreal Patagonia of Chile. Zootaxa 2007, 1452:25-42.
75. Posada D. JModelTest: phylogenetic model averaging. Molecular Biology and Evolution 2008, 25:1253-1256.
76. Rabassa J., Clapperton C.M. Quaternary glaciations in the southern Andes. Quaternary Science Reviews 1990, 9:153-174.
77. Redenbach Z., Taylor E.B. Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America. Evolution 2002, 56:1021-1035.
78. Renaud S., Alibert P., Auffray J.C. Mandible shape in hybrid mice. Naturwissen-schaften 2009, 96:1043-1050.
79. Rieppel O. Species as a process. Acta Biotheoretica 2009, 57:33-49.
80. Rieseberg, L.H., Wendel, J., 1993. Introgression and its Consequences in Plants. Edition R. Harrison. Oxford University Press, New York. pp. 70-1114.
81. Rieseberg L.H., Sinervo B., Linder C.R., Ungerer M.C., Arias D.M. Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science 1996, 272:741-745.
82. Rieseberg L.H., Whitton J., Linder C.R. Molecular marker incongruence in plant hybrid zones and phylogenetic trees. Acta Botanica Neerlandica 1996, 45:243-262.
83. Rieseberg L.H., Archer M.A., Wayne R.K. Transgressive segregation, adaptation and speciation. Heredity 1999, 83:363-372.
84. Ronquist F., Huelsenbeck J.P. Mr Bayes version 3: bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
85. Rosenberg N.A. The probability of topological concordance of gene trees and species trees. Theoretical Population Biology 2002, 61:225-247.
86. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 1999, 15:174-175.
87. Ruzzante D.E., Walde S.J., Gosse J.C., Cussac V.E., Habit E., Zemlak T.S., Adams E.D.M. Climate control on ancestral population dynamics: insight from patagonian fish phylogeography. Molecular Ecology 2008, 17:2234-2244.
88. Seehausen O. Hybridization and adaptive radiation. Trends in Ecology & Evolution 2004, 19:198-207.
89. Smith M.F., Thomas W.K., Patton J.L. Mitochondrial DNA-like sequence in the nuclear genome of an akodontine rodent. Molecular Biology and Evolution 1992, 9:204-215.
90. Sullivan J.P., Lavaqué S., Hopkins C.D. Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 2002, 56:597-616.
91. Tajima F. Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
92. Than C., Nakhleh L. Species tree inference by minimizing deep coalescences. PLoS Computational Biology 2009, 5:e1000501. 10.1371/journal.pcbi.1000501.
93. Than C., Nakhleh L. Inference of parsimonious species phylogenies from multi-locus data by minimizing deep coalescences. Estimating Species Trees: Practical and Theoretical Aspects 2010, 79-98. Wiley-VCH. L.L. Knowles, L.S. Kubatko (Eds.).
94. Than C., Ruth D., Nakhlek L. PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 2008, 9:322.
95. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 1997, 25:4876-4882.
96. Vega L., Bellagamba P. Ciclo reproductivo de Liolaemus gracilis Bell, 1843 (Iguanidae: Tropidurinae) en las dunas costeras de Buenos Aires. Argentina. Cuadernos de Herpetología 2005, 18:3-13.
97. Vega L., Bellagamba P., Lobo F. A new endemic species of Liolaemus (Iguania: Liolaemidae) from the mountain range of Tandilia, Buenos Aires province, Argentina. Herpetologica 2008, 64(1):59.
98. Vitt L.J., Cooper W.E. The evolution of sexual dimorphism in the skink Eumeces laticeps: an example of sexual selection. Canadian Journal of Zoology 1985, 63:995-1002.
99. Wiens J.J., Penkrot T.A. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizard (Sceloporus). Systematic Biology 2002, 51:69-91.
100. Wright S. Evolution in Mendelian populations. Genetics 1931, 16:97-159.