Strong selection against hybrids maintains a narrow contact zone between morphologically cryptic lineages in a rainforest lizard

Evolution

Volumn 66, Issue 5, 2012, Pages 1474-1489

  Singhal, Sonal ^a   Moritz, Craig ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hybrid zones; Lampropholis coggeri; Phylogeography; Simulations; Speciation

Indexed keywords

MITOCHONDRIAL DNA;

BIODIVERSITY; CONTACT ZONE; HYBRID; LIZARD; MORPHOLOGY; NATURAL SELECTION; NUMERICAL MODEL; PHYLOGEOGRAPHY; RAINFOREST; REPRODUCTIVE ISOLATION; SELECTION;

ANIMAL; ARTICLE; AUSTRALIA; BIOLOGICAL MODEL; CELL NUCLEUS; CLASSIFICATION; FEMALE; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; HYBRIDIZATION; LIZARD; MALE; PHYLOGEOGRAPHY; POLYMERASE CHAIN REACTION; REPRODUCTIVE ISOLATION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL;

ANIMALS; CELL NUCLEUS; DNA, MITOCHONDRIAL; FEMALE; GENETIC VARIATION; HYBRIDIZATION, GENETIC; LIKELIHOOD FUNCTIONS; LIZARDS; MALE; MODELS, GENETIC; PHYLOGEOGRAPHY; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; POLYMORPHISM, SINGLE NUCLEOTIDE; QUEENSLAND; REPRODUCTIVE ISOLATION; SELECTION, GENETIC;

LAMPROPHOLIS COGGERI; SQUAMATA;

EID: 84860195279     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01539.x     Document Type: Article

References (102)

1. Alexandrino, J., S. Baird, L. Lawson, J. Macey, C. Moritz, and D. Wake 2005. Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution 59:1334-1347.
2. Aljanabi, S., and I. Martinez 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nuc. Acids Res. 25: 4692-4693.
3. Anderson, E., and E. Thompson 2002. A model-based method for identifying species hybrids by using multilocus genetic data. Genetics 160: 1217-1229.
4. Arevalo, E., S. Davis, and J. Sites 1994. Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phyrnosomatidae) in Central Mexico. Sys. Bio. 43: 387-418.
5. Arnold, M. 1997. Natural hybridization and evolution. Oxford Univ. Press, Oxford, UK
6. Avise, J. 2000. Phylogeography: the history and formation of species. Harvard University, Cambridge, MA
7. Avise, J., and K. Wollenberg 1997. Phylogenetics and the origin of species. Proc. Natl. Acad. Sci. 94: 7748-7755.
8. Baird, S. 1995. A simulation study of multilocus clines. Evolution 49: 1038-1045.
9. Barton, N. 1979. Gene flow past a cline. Heredity 43: 333-339.
10. Barton, N. 1983. Multilocus clines. Evolution 37: 454-471.
11. Barton, N. 2000. Estimating multilocus linkage disequilibria. Heredity 84: 373-389.
12. Barton, N., and S. Baird 1998. Analyse 1.10. Available at
13. Barton, N., and K. Gale 1993. Genetic analysis of hybrid zones. Pp. 13-45 in R. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, UK
14. Bazykin, A.. 1969. A hypothetical mechanism of speciation. Evolution 23: 685-687.
15. Bell, R., J. Parra, M. Tonione, C. Hoskin, J. MacKenzie, S. Williams, and C. Moritz 2010. Patterns of persistence and isolation indicate resilience to climate change in montane rainforest lizards. Mol. Ecol. 19: 2531-2544.
16. Bentley, D., S. Balasubramanian, H. P. Swerdlow, G. P. Smith, J. Milton, C. G. Brown, K. P. Hall, D. J. Evers, C. L. Barnes, H. R. Bignell, et al. 2006. Accurate whole genome sequencing using reversible terminator chemistry. Nature 456:53-59.
17. Bickford, D., D. Lohman, N. Sodhi, P. Ng, R. Meier, K. Winker, K. Ingram, and I. Das 2006. Cryptic species as a window on diversity and conservation. TREE 22: 148-155.
18. Birney, E., and the Ensembl Team. 2003. Ensembl: a genome infrastructure. Cold Spring Harb. Symp. Quant. Biol. 68:213-216.
19. Biron, I., S. Jackman, C. Nielsen, J. Qian, R. Varhol, G. Stazyk, R. Morin, Y. Zhao, M. Hirst, J. Schein, et al 2009. De novo transcriptome assembly with ABySS. Bioinformatics 25: 2872-2877.
20. Bond, J., and A. Stockman 2008. An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring. Sys. Bio. 57: 628-646.
21. Brumfield, R., R. Jernigan, D. McDonald, and M. Braun 2001. Evolutionary implications of divergent clines in an avian (Manacus, Aves) hybrid zone. Evolution 55: 2070-2087.
22. Buno, I., E. Torroja, C. Lopezfernandez, R. Butlin, G. Hewitt, and J. Gosalvez 1994. A hybrid zone between two subspecies of the grasshopper Chorthippus parallelus along the Pyrenees-the west end. Heredity 73: 625-634.
23. Carling, M., and R. Brumfield 2008. Haldane's rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal and sex-linked loci across the Passerina bunting hybrid zone. Evolution 62: 2600-2615.
24. Carling, M., and R. Brumfield 2009. Speciation in Passerina buntings: introgression patterns of sex-linked loci identify a candidate gene region for reproductive isolation. Mol. Ecol. 18: 834-847.
25. Coyne, J., and H. Orr 1997. Patterns of speciation in Drosophila revisited. Evol. 51: 295-303.
26. Cruzan, M., and M. Arnold 1994. Assortative mating and natural selection in an Iris hybrid zone. Evolution 48: 1946-1958.
27. Dasmahapatra, K., M. Blum, A. Aiello, S. Hackwell, N. Davies, E. Bermingham, and J. Mallet 2002. Inferences from a rapidly moving hybrid zone. Evolution 56: 741-753.
28. Dolman, G. 2009. Evidence for differential assortative female preference in association wth refugial isolation of rainbow skinks in Australia's tropical rainforests. PLoS ONE 3:e3499.
29. Dolman, G., and B. Phillips 2004. Single copy nuclear DNA markers characterized for comparative phylogeography in Australian wet tropics rainforest skinks. Mol. Ecol. Notes 4: 185-187.
30. Dufkova, P., M. Macholan, and J. Pialek 2011. Inference of selection and stochastic effects in the house mouse hybrid zone. Evolution 65: 993-1010.
31. Durrett, R., L. Buttel, and R. Harrison 2000. Spatial models for hybrid zones. Heredity 84: 9-19.
32. Earl, D. 2011. Structure harvester v0.6.6. Available at
33. Endler, J. 1977. Geographic variation, speciation and clines. Princeton, Princeton, NJ
34. Evanno, G., S. Regnaut, and J. Goudet 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-20.
35. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35: 124-138.
36. Fujita, M., J. McGuire, S. Donnellan, and C. Moritz 2010. Diversifiation and persistence at the arid-monsoonal interface: Australia-wide biogeography of the Bynoe's Gecko (Heteronotia binoei, Gekkonidae). Evolution 64: 2293-2314.
37. Futuyma, D. 2010. Evolutionary constraints and ecological consequences. Evolution 64: 1865-1884.
38. Gavrilets, S., 1997. Hybrid zones with Dobzhansky-type epistatic selection. Evol. 51:1027-1035.
39. Gavrilets, S. and M. Cruzan 1998. Neutral gene flow across single locus clines. Evolution 52: 1277-1284.
40. Gay, L., P. Crochet, D. Bell, and T. Lenormand 2008. Comparing clines on molecular and phenotypic traits in hybrid zones: a window on tension zone models. Evolution 18: 1-18.
41. Gomez, A., M. Serra, G. Carvalho, and D. Lunt 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56: 1431-1444.
42. Graham, C., C. Moritz, and S. Williams 2006. Habitat history improves prediction of biodiversity in rainforest fauna. Proc. Natl. Acad. Sci. USA 103: 632-636.
43. Grundt, H., S. Kjolner, L. Borgen, L. Rieseberg, and C. Brochmann 2006. High biological species diversity in the artic flora. Proc. Natl. Acad. Sci. 103: 972-975.
44. Haas, F., J. Knape, and A. Brodin 2010. Habitat preferences and positive assortative mating in an avian hybrid zone. J. Avian Bio. 41: 237-247.
45. Harrison, R. 1986. Pattern and process in a narrow hybrid zone. Heredity 56: 337-349.
46. Harrison, R. 1993. Hybridization and hybrid zones: historical perspective. Pp. 3-12 in Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, UK
47. Hebert, P., E. Penton, J. Burns, D. Janzen, and W. Hallwachs 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA 101: 14812-14817.
48. Hewitt, G. 2011. Quaternary phylogeography: the roots of hybrid zones. Genetica 139: 617-638.
49. Hoskin, C., M. Higgie, K. McDonald, and C. Moritz 2005. Reinforcement drives rapid allopatric speciation. Nature 437: 1353-1356.
50. Jakobsson, M., and N. Rosenberg 2007. CLUMPP: a cluster matching and permutation program for dealing with multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
51. Janzen, D. 1967. Why mountain passes are higher in the tropics. Am. Nat. 101:233-249.
52. Jiggins, C., and J. Mallet 2000. Bimodal hybrid zones and speciation. TREE 15: 250-255.
53. Kawakami, T., R. Butlin, M. Adams, D. Paull, and S. Cooper 2009. Genetic analysis of a chromosomal hybrid zone in the Australian grasshoppers (Vandiemenella, viatica species group). Evol. 63: 139-152.
54. Kruuk, L., S. Baird, K. Gale, and N. Barton 1999. A comparison of multilocus clines maintained by environmental selection or by selection against hybrids. Genetics 153: 1959-1971.
55. Leache, A., and M. Fujita 2010. Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proc. R. Soc. Lond. B 277: 3071-3077.
56. Li, H., and R. Durbin 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
57. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. HOmer, G. Marth, G. Abecasis, R. Durbin, and 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25: 2078-2079.
58. Maccallum, C., B. Nurenberger, and N. Barton 1995. Experimental evidence for habitat dependent selection in a Bombina hybrid zone. Proc. Bio. Sci. 260: 257-264.
59. Macholan, M., P. Munclinger, M. Sugerkova, P. Dukova, B. Bimova, E. Bozikova, J. Zima, and J. Pialek 2007. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61: 746-771.
60. Mallet, J., N. Barton, G. Lamas, J. Santisteban, M. Muedas, and H. Eeley 1990. Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124: 921-936.
61. Mani, G., and B. Clarke 1990. Mutational order: a major stochastic process in evolution. Proc. R. Soc. Lond. B 240: 29-37.
62. Mettler, R., and G. Spellman 2009. A hybrid zone revisited : molecular and morphological analysis of the maintenance, movement, and evolution of a Great Plains avian (Cardinalidae: Pheucticus) hybrid zone. Mol. Ecol. 18: 3256-3267.
63. M'Gonigle, L., and R. FitzJohn 2009. Assortative mating and spatial structure in hybrid zones. Evolution 64: 444-455.
64. Moore, W. 1977. An evaluation of narrow hybrid zones in vertebrates. Quat. Rev. Bio. 52: 263-277.
65. Moore, W. 2008. Assortative mating genes selected along a gradient. Heredity 25: 2241-2246.
66. Moore, W., and J. Price 1993. Nature of selection in the northern flicker hybrid zone and its implications for speciation theory. Pp. 196-225 in R. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, UK
67. Moritz, C., C. Hoskin, J. MacKenzie, B. Phillips, M. Tonione, N. Silva, J. VanDerWal, S. Williams, and C. Graham 2009. Identification and dynamics of a cryptic suture zone in a tropical rainforest. Proc. R. Soc. Lond. B 276: 1235-1244.
68. Nix, H. 1991. Biogeography: patterns and process. Pp. 11-40 in H. A. Nix and M. Switzer, eds. Rainforest animals: atlas of vertebrates endemic to Australia's Wet Tropics. Australian Nature Conservation Agency, Canberra
69. Nosil, P., and S. Flaxman 2011. Conditions for mutation order speciation. Proc. R. Soc. Lond. B. 278: 399-407.
70. Patton, J. 1993. Hybridization and hybrid zones in pocket gophers (Rodentia, Geomyidae). Pp. 290-308 in R. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, UK
71. Peng, B., and M. Kimmal 2005. simuPOP: a forward-time population genetics simulation environment. Bioinformatics 21: 3686-3687.
72. Pereira, R., and D. Wake, 2009. Genetic leakage after adaptive and nonadaptive divergence in the Ensatina eschscholtzii ring species. Evolution 63:2288-2301.
73. Phillips, B., S. Baird, and C. Moritz 2004. When vicars meet: a narrow contact zone between morphologically cryptic phylogeographic lineages of the rainforest skink, Carlia rubrigularis. Evolution 58: 1536-1548.
74. Pool, J., and R. Nielsen 2009. Inference of historical changes in migration rate from the lengths of migrant tracts. Genetics 181: 711-719.
75. Pope, L., A. Estoup, and C. Moritz 2000. Phylogeography and population structure of an ecotonal marsupial, Bettongia tropica, determined using mtDNA and microsatellites. Mol. Ecol. 9: 2041-2053.
76. Porter, A., R. Wenger, H. Geiger, A. Scholl, and A. Shapiro 1997. The Pontia daplidice-edusa hybrid zone in northwestern Italy. Evolution 52: 1561-1573.
77. Pritchard, J., M. Stephens, and P. Donnelly 2000. Inference of population structure suing multilocus genotype data. Genetics 145: 945-959.
78. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Available at ISBN 3-900051-07-0.
79. Rissler, L., and J. Apodaca 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Sys. Bio. 57: 924-942.
80. Rosenberg, N. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Res. 4: 137-138.
81. Rousset, F.. 1997. Genetic differentiation and estimation of gene flow from f-statistics under isolation by distance. Genetics 145: 1219-1228.
82. Rozen, S., and H. Skaletsky 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
83. Sadedin, S., and M. Littlejohn 2003. A spatially explicit individual-based model of reinforcement in hybrid zones. Evolution 57: 962-970.
84. Saetre, G., T. Moum, S. Bures, M. Kral, M. Adamjan, and J. Moreno 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387: 589-592.
85. Sequeira, F., J. Alexandrino, S. Rocha, J. Arntzen, and N. Ferrand 2005. Genetic exchange across a hybrid zone within the iberian endemic golden striped salamander, Chiloglossa lusitanica. Mol. Ecol. 14: 245-254.
86. Shaw, A. 2000. Molecular phylogeography and cyrptic speciation in the mosses Mielichhoferia elongata and M. mielicchoferiana (Bryaceae). Mol. Ecol.9: 595-608.
87. Sites, J., N. Barton, and K. Reed 1995. The genetic structure of a hybrid zone between two chromosome races of the Sceloporus grammicus complex (Sauria, Phrynosomatidae) in central Mexico. Evolution 49: 9-36.
88. Smadja, C., and R. Butlin 2009. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102: 77-97.
89. Stuart-Fox, D., R. Godinho, J. G. de Bellocq, N. Irwin, J. Brito, A. Moussalli, P. Siroky, A. Hugall, and S. Baird 2009. Variation in phenotype, parasite load and male competitve ability across a cryptic hybrid zone. PLoS ONE 4:e5677.
90. Sumner, J., F. Rousset, A. Estoup, and C. Moritz 2001. Neighbourhood size, dispersal and desnity estimates of the prickly forest skink (Gnypetoscincus queenslandiae) usng individual genetic and demographic methods. Mol. Ecol. 10: 1917-1927.
91. Sunderland, M. Teaching natural history at the Museum of Vertebrate Zoology. Br. J. Hist. Sci. doi:.
92. Szymura, J., and N. Barton 1986. Genetic analysis of a hybrid zone between the fire-bellied toads Bombina bombina and B. variegata, near Cracow in Southern Poland. Evolution40: 1141-1159.
93. Szymura, J., and N. Barton 1991. The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution45: 237-261.
94. Teeter, K., B. Payseur, L. Harris, M. Bakewell, L. Thibodeau, J. O'Brien, J. Krenz, M. Sans-Fuentes, M. Nachman, and P. Tucker 2008. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18: 1-10.
95. VanDerWal, J., L. Shoo, and S. Williams 2009. New approaches to understanding late Quaternary climate fluctuations and refugial dynamics in Australian tropical rain forests. J. Biogeogr. 36: 291-301.
96. Wake, D. 2006. Problems with species: patterns and processes of species formation in salamanders. Ann. Mo Bot. Gard. 93: 8-23.
97. Weir, J., and T. Price 2011. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177: 462-469.
98. Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York Available at
99. Wiley, C., A. Qvarnstrom, G. Andersson, T. Borge, and G. Saetre 2009. Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution 63:1731-1739.
100. Williams, S., J. VanDerWal, J. Isaac, L. Shoo, C. Storlie, S. Fox, E. Bolitho, C. Moritz, C. Hoskin, and Y. Williams 2010. Distributions, life history characteristics, ecological specialization and phylogeny of the rainforest vertebrates in the Australian Wet Tropics bioregion. Ecology 91: 2493.
101. Yanchukov, A., S. Hofman, J. S. S. Mezhzherin, S. Morozov-Leonov, N. Barton, and B. Numberger 2006. Hybridization of Bombina bombina and B. variegata (Anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution60: 583-600.
102. Yuri, T., R. Jernigan, R. Brumfield, N. Bhagabati, and M. Braun 2009. The effect of marker choice on estimated levels of introgression across an avian (Pipridae: Manacus) hybrid zone. Mol. Ecol. 18: 4888-4903.