Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times

BMC Biology

Volumn 8, Issue , 2010, Pages

  Elmer, Kathryn R ^a   Lehtonen, Topi K ^a,b   Kautt, Andreas F ^a   Harrod, Chris ^c,d   Meyer, Axel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MONASH UNIVERSITY   (Australia)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHILOPHUS; AMPHILOPHUS CITRINELLUS; CICHLIDAE; PISCES;

FRESH WATER; MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CICHLID; DNA SEQUENCE; ECOSYSTEM; EVOLUTION; GENE FREQUENCY; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; HISTOLOGY; MOLECULAR GENETICS; MORPHOMETRICS; NICARAGUA; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POPULATION GENETICS; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; VOLCANO;

ADAPTATION, BIOLOGICAL; ANIMALS; BASE SEQUENCE; BODY WEIGHTS AND MEASURES; CICHLIDS; DNA, MITOCHONDRIAL; ECOSYSTEM; EVOLUTION; FRESH WATER; GENE FREQUENCY; GENETIC SPECIATION; GENETIC VARIATION; GENETICS, POPULATION; HAPLOTYPES; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NICARAGUA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; VOLCANIC ERUPTIONS;

EID: 77951990776     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-60     Document Type: Article

References (115)

1. Losos JB, Ricklefs RE. Adaptation and diversification on islands. Nature 2009, 457:830-836. 10.1038/nature07893, 19212401.
2. Grant PR, Grant BR. Adaptive radiation of Darwin's finches: Recent data help explain how this famous group of Galapagos birds evolved, although gaps in our understanding remain. Am Sci 2002, 90:130-141.
3. Savolainen V, Anstett MC, Lexer C, Hutton I, Clarkson JJ, Norup VV, Powell MP, Springate D, Salamin N, Baker WJ. Sympatric speciation in palms on an oceanic island. Nature 2006, 441:210-213. 10.1038/nature04566, 16467788.
4. Barluenga M, Stölting KN, Salzburger W, Muschick M, Meyer A. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 2006, 439:719-723. 10.1038/nature04325, 16467837.
5. Gavrilets S, Vose A, Barluenga M, Salzburger W, Meyer A. Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake. Mol Ecol 2007, 16:2893-2909. 10.1111/j.1365-294X.2007.03305.x, 17614905.
6. Schliewen U, Rassmann K, Markmann M, Markert J, Kocher TD, Tautz D. Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions. Mol Ecol 2001, 10:1471-1488. 10.1046/j.1365-294X.2001.01276.x, 11412369.
7. Schliewen UK, Tautz D, Paabo S. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 1994, 368:629-632. 10.1038/368629a0, 8145848.
8. Schluter D. The Ecology of Adaptive Radiations. 2000, New York: Oxford University Press.
9. Nosil P, Harmon LJ, Seehausen O. Ecological explanations for (incomplete) speciation. Trends Ecol Evol 2009, 24:145-156. 10.1016/j.tree.2008.10.011, 19185951.
10. Waxman D, Gavrilets S. 20 questions on adaptive dynamics. J Evol Biol 2005, 18:1139-1154. 10.1111/j.1420-9101.2005.00948.x, 16135102.
11. Orr MR, Smith D. Ecology and speciation. Trends Ecol Evol 1998, 13:502-506.
12. Schluter D. Ecological speciation in postglacial fishes. Phil Trans R Soc B 1996, 351:807-814.
13. McKinnon JS, Rundle H. Speciation in nature: the threespine stickleback model system. Trends Ecol Evol 2002, 17:480-488.
14. Hendry AP, Wenburg JK, Bentzen P, Volk EC, Quinn TP. Rapid evolution of reproductive isolation in the wild: Evidence from introduced salmon. Science 2000, 290:516-518. 10.1126/science.290.5491.516, 11039932.
15. Lu G, Bernatchez L. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution 1999, 59:1491-1505.
16. Østbye K, Amundsen PA, Bernatchez L, Klemetsen A, Knudsen R, Kristoffersen R, TF N, Hindar K. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol Ecol 2006, 15:3983-4001. 10.1111/j.1365-294X.2006.03062.x, 17054498.
17. Meyer A. Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 1993, 8:279-285.
18. Salzburger W. The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 2009, 18:169-185. 10.1111/j.1365-294X.2008.03981.x, 18992003.
19. Barlow GW. The Midas cichlid in Nicaragua. Investigations of the Ichthyology of Nicaraguan Lakes 1976, 333-358. Lincoln: University of Nebraska Press, Thorson TB.
20. Barlow GW, Munsey JW. The red devil-Midas-arrow cichlid species complex in Nicaragua. Investigations of the Ichthyology of Nicaraguan Lakes 1976, 359-369. Lincoln: University of Nebraska Press, Thorson TB.
21. Meyer A. Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. J Zool 1990, 221:237-260.
22. Elmer KR, Kusche H, Lehtonen TK, Meyer A. Local variation and parallel evolution: morphological and genetic diversity across a species complex of Neotropical crater lake cichlid fishes. Phil Trans R Soc B 2010, 365:1769-1782.
23. Bunje PME, Barluenga M, Meyer A. Sampling genetic diversity in the sympatrically and allopatrically speciating Midas cichlid species complex over a 16 year time series. BMC Evol Biol 2007, 7:25. 10.1186/1471-2148-7-25, 1819369, 17311680.
24. Barluenga M, Meyer A. The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes?. Mol Ecol 2004, 13:2061-2076. 10.1111/j.1365-294X.2004.02211.x, 15189226.
25. Elmer KR, Lehtonen TK, Meyer A. Color assortative mating contributes to sympatric divergence of neotropical crater lake cichlid fish. Evolution 2009, 63:2750-2757. 10.1111/j.1558-5646.2009.00736.x, 19490078.
26. McKaye KR, Stauffer JR, Berghe EP, Vivas R, Perez LJL, McCrary JK, Waid R, Konings A, Lee WJ, Kocher TD. Behavioral, morphological and genetic evidence of divergence of the Midas cichlid species complex in two Nicaraguan crater lakes. Cuadernos Investigación UCA 2002, 12:19-47.
27. Kutterolf K, Freundt A, Pérez W, Wehrmann H, Schmincke HU. Late Pleistocene to Holocene temporal succession and magnitudes of highly-explosive volcanic eruptions in west-central Nicaragua. J Volcanol Geotherm Res 2007, 163:55-82.
28. Volcan Apoyeque. , http://www.ineter.gob.ni/geofisica/vol/apoyeque/index.html
29. Laguna Apoyeque. , http://www.ineter.gob.ni/Direcciones/Recursos%20Hidricos/HIDROGRAFIA%20WEB/Lagunas/Apoyeque.htm
30. Waid RM, Raesly RL, McKaye KR, McCrary JK. Zoogeografía íctica de lagunas cratéricas de Nicaragua. Encuentro 1999, 51:65-80.
31. Barlow GW, Baylis JR, Roberts D. Chemical analyses of some crater lakes in relation to adjacent Lake Nicaragua. Investigations of the Ichthyology of Nicaraguan Lakes 1976, 17-20. Lincoln: University of Nebraska Press, Thorson TB.
32. Beerli P, Felsenstein J. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 1999, 152:763-773. 1460627, 10353916.
33. Beerli P, Felsenstein J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 2001, 98:4563-4568. 10.1073/pnas.081068098, 31874, 11287657.
34. Wallace RK. An assessment of diet-overlap indexes. Trans Am Fish Soc 1981, 110:72-76.
35. McCrary JK, Madsen H, Gonzáles L, Luna I, López LJ. Comparison of gastropod mollusc (Apogastropoda: Hydrobiidae) habitats in two crater lakes in Nicaragua. Rev Biol Trop 2008, 56:113-120.
36. Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83:703-718.
37. Vivas R, McKaye KR. Habitat selection, feeding ecology, and fry survivorship in the Amphilophus citrinellus species complex in Lake Xiloá. J Aquacult Aq Sci 2001, IX:32-48.
38. Meyer A. Costs and benefits of morphological specialization: feeding performance in the trophically polymorphic neotropical cichlid fish, Cichlasoma citrinellum. Oecologia 1989, 80:431-436.
39. Meyer A. Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol J Linn Soc 1990, 39:279-299.
40. Greenwood PH. Environmental effects on the pharyngeal mill of a cichild fish, Astatoreochromis alluaudi and their taxonomic implications. Proc Linn Soc Lond 1965, 176:1-10.
41. Klingenberg CP, Barluenga M, Meyer A. Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex. Biol J Linn Soc 2003, 80:397-408.
42. Rueffler C, Van Dooren TJM, Leimar O, Abrams PA. Disruptive selection and then what?. Trends Ecol Evol 2006, 21:238-245. 10.1016/j.tree.2006.03.003, 16697909.
43. Martin RA, Pfennig DW. Disruptive selection in natural populations: the roles of ecological specialization and resource competition. Am Nat 2009, 174:268-281. 10.1086/600090, 19527118.
44. Hendry AP, Grant PR, Grant BR, Ford HA, Brewer MJ, Podos J. Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches. Proc R Soc Lond B 2006, 273:1887-1894.
45. Schluter D, McPhail JD. Ecological character displacement and speciation in sticklebacks. Am Nat 1992, 140:85. 10.1086/285404, 19426066.
46. Bolnick DI. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 2004, 58:608-618.
47. Udovic D. Frequency-dependent selection, disruptive selection, and the evolution of reproductive isolation. Am Nat 1980, 116:621-641.
48. Pennings PS, Kopp M, Meszéna G, Dieckmann U, Hermisson J. An analytically tractable model for competitive speciation. Am Nat 2008, 171:E44-E71. 10.1086/523952, 18171142.
49. Keenleyside MHA. Cichlid Fishes: Behaviour, Ecology and Evolution. 1991, London: Chapman and Hall.
50. de Lucena CAS, Kullander SO. The Crenicichla (Teleostei: Cichlidae) species of the Uruguai River drainage in Brazil. Ichthyol Explor Fres 1992, 3:97-192.
51. Arnegard ME, Snoeks J. New three-spotted cichlid species with hypertrophied lips (Teleostei: Cichlidae) from the deep waters of Lake Malawi/Nyasa, Africa. Copeia 2001, 2001:705-717.
52. Kocher TD, Conroy JA, McKaye KR, Stauffer JR. Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol Phylogen Evol 1993, 2:158-165.
53. Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR, Turner GF. Age of cichlids: new dates for ancient lake fish radiations. Mol Biol Evol 2007, 24:1269-1282. 10.1093/molbev/msm050, 17369195.
54. Renesto E, Zawadzki CH, Revaldaves E. Biochemical taxonomy of Crenicichla (Pisces: Perciformes: Cichlidae) of the Iguaçu River, Brazil. Braz Arch Biol Techn 2001, 44:15-22.
55. Kullander SO, Norén M, Frioriksson GB, de Lucena CAS. Phylogenetic relationships of species of Crenicichla (Teleostei: Cichlidae) in southern South America based on the mitochondrial cytochrome b gene. J Zool Syst Evol Res [doi: 10.1111/j.1439-0469.2009.00557.x].
56. Villa J. Systematic status of the cichlid fishes Cichlasoma dorsatum, C. granadense and C. nigritum Meek. Investigations of the Ichthyology of Nicaraguan Lakes 1976, 101-113. Lincoln: University of Nebraska Press, Thorson TB.
57. Elmer KR, Fan S, Gunter HM, Jones JC, Boekhoff S, Kuraku S, Meyer A. Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes. Mol Ecol 2010, 19(Suppl 1):197-211. 10.1111/j.1365-294X.2009.04488.x, 20331780.
58. Gavrilets S. Fitness Landscapes and the Origin of Species. 2004, Princeton: Princeton University Press.
59. Maynard Smith J. Sympatric speciation. Am Nat 1966, 100:637-650.
60. Thibert-Plante X, Hendry AP. Five questions on ecological speciation addressed with individual-based simulations. J Evol Biol 2009, 88:109-123.
61. Stauffer JR, McKaye KR. Descriptions of three new species of cichlid fishes (Teleostei: Cichlidae) from Lake Xiloá, Nicaragua. Cuadernos Investigación UCA 2002, 12:1-18.
62. Hey J, Won YJ, Sivasundar A, Nielsen R, Markert J. Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol 2004, 13:909-919. 10.1046/j.1365-294X.2003.02031.x, 15012765.
63. Won YJ, Sivasundar A, Wang Y, Hey J. On the origin of Lake Malawi cichlid species: A population genetic analysis of divergence. Proc Natl Acad Sci USA 2005, 102:6581-6586. 10.1073/pnas.0502127102, 1131877, 15851665.
64. Thomson DP. Introduction to Meterology. 1849, London: William Blackwood and Sons.
65. Hora SL. Catching fishes with the hand in India. Science 1950, 11:263-264.
66. Villa J. Ichthyology of the Lakes of Nicaragua: historical perspective. Investigations of the Ichthyology of Nicaraguan Lakes 1976, 101-113. Lincoln: University of Nebraska Press, Thorson TB.
67. Brinton DG. On an ancient human footprint from Nicaragua. Proc Am Phil Soc 1887, 24:437-444.
68. Caliro S, Chiodini G, Izzo G, Minopli C, Signorini A, Avino R, Granieri D. Geochemical and biochemical evidence of lake overturn and fish kill at Lake Averno, Italy. J Volcanol Geotherm Res 2008, 178:305-316.
69. Tassi F, Vaselli O, Fernandez E, Duarte E, Martinez M, Delgado Huertas A, Bergamaschi F. Morphological and geochemical features of crater lakes in Costa Rica: an overview. J Limnol 2009, 68:193-205.
70. Mayr E. Change of genetic environment and evolution. Evolution as a Process 1954, 157-180. New York: Collier Books, Huxley J, Hardy AC, Ford EB.
71. Barrett RDH, Schluter D. Adaptation from standing genetic variation. Trends Ecol Evol 2007, 23:38-44. 10.1016/j.tree.2007.09.008, 18006185.
72. Gavrilets S, Vose A. Dynamic patterns of adaptive radiation. Proc Natl Acad Sci USA 2005, 102:18040. 10.1073/pnas.0506330102, 1312382, 16330783.
73. Doebeli M. A quantitative genetic competition model for sympatric speciation. J Evol Biol 1996, 9:893-909.
74. Pearse DE, Hayes SA, Bond MH, Hanson CV, Anderson EC, Macfarlane RB, Garza JC. Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss). J Hered 2009, 100:515-525. 10.1093/jhered/esp040, 19561050.
75. Hart JJ, Gross MR, Heino M, Hilborn R, Kope RG, Law R, Reynolds JD. Evolutionary consequences of fishing and their implications for salmon. Evol Appl 2008, 1:388-408.
76. Hendry AP, Nosil P, Rieseberg LH. The speed of ecological speciation. Funct Ecol 2007, 21:455-464. 10.1111/j.1365-2435.2007.01240.x, 2605086, 19096732.
77. Rasband WS. ImageJ. 1997, Bethesda: US National Institutes of Health., http://rsb.info.nih.gov/ij/
78. Rohlf FJ. TPSDig2: a program for landmark development and analysis. 2007, New York: Department of Ecology and Evolution, State University of New York, Stony Brook., http://life.bio.sunysb.edu/morph/
79. Klingenberg CP. MorphoJ. 2008, Manchester: Faculty of Life Sciences, Univ. of Manchester., http://www.flywings.org.uk/MorphoJ_page.htm
80. Dryden IL, Mardia KV. 1998, Statistical Shape Analysis Chichester: Wiley.
81. Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 2002, 56:1909-1920.
82. Hyslop EJ. Stomach contents analysis-a review of methods and their application. J Fish Biol 1980, 17:411-429.
83. Schoener TW. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 1970, 51:408-418.
84. Harrod C, Grey J. Isotopic variation complicates analysis of trophic relations within the fish community of Plußsee: a small, deep, stratifying lake. Arch Hydrobiol 2006, 167:281-299.
85. Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI. A revised model for lipid-normalising d13C values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 2006, 43:1213-1222.
86. Hammer T, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 2001, 41:9.
87. SAS JMP Statistical Discovery version 7 2007, NC, USA: SAS Institute Inc, SAS.
88. Brewer MJ. Discretisation for inference on normal mixture models. Stat Comput 2003, 13:209-219.
89. Burnham KP, Anderson DR. Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach. 2002, New York: Springer-Verlag, Inc.
90. Petit RJ, El Mousadik A, Pons O. Identifying populations for conservation on the basis of genetic markers. Conserv Biol 1998, 12:844-855.
91. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497. 10.1093/bioinformatics/btg359, 14668244.
92. Excoffier L, Laval LG, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
93. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C content biases. Mol Biol Evol 1992, 9:678-687.
94. Hasewaga M, Kishino H, Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985, 22:160-174. 10.1007/BF02101694, 3934395.
95. Posada D, Crandall K. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818. 10.1093/bioinformatics/14.9.817, 9918953.
96. Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. 2003, Sunderland: Sinauer Associates.
97. Bandelt HJ, Forester P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
98. Posada D, Crandall KA. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 2001, 16:37-45. 10.1016/S0169-5347(00)02026-7, 11146143.
99. Sanetra M, Henning F, Fukamachi S, Meyer A. A microsatellite-based genetic linkage map of the cichlid fish, Astatotilapia burtoni (Teleostei): A comparison of genomic architectures among rapidly speciating cichlids. Genetics 2009, 182:387-397. 10.1534/genetics.108.089367, 2674835, 18757932.
100. Noack K, Wilson AB, Meyer A. Broad taxonomic applicability of microsatellites developed for the highly polymorphic neotropical cichlid, Amphilophus citrinellum. Anim Genet 2000, 31:151-152. 10.1046/j.1365-2052.2000.00592.x, 10782229.
101. Kellogg KA, Markert JA, Stauffer JR, Kocher TD. Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proc R Soc Lond B 1995, 260:79-84.
102. Salzburger W, Braasch I, Meyer A. Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes. BMC Biol 2007, 5:51. 10.1186/1741-7007-5-51, 2254590, 18005399.
103. Zardoya R, Vollmer DM, Craddock C, Streelman JT, Karl S, Meyer A. Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proc R Soc Lond B 1996, 263:1589-1598.
104. van Oosterhout C, Hutchison WF, Wills DPM, Shipley P. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
105. Brookfield JFY. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 1996, 5:453-455.
106. Dieringer D, Schlötter C. Microsatellite Analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 2003, 3:167-169.
107. Kalinowski ST. Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conserv Genet 2004, 5:539-543.
108. Kalinowski ST. HP-Rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 2005, 5:187-189.
109. Raymond M, Rousset F. An exact test for population differentiation. Evolution 1995, 49:1280-1283.
110. Rousset F. Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 2008, 8:103-106.
111. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. GENETIX 4.05, Logiciel Sous Windows TM Pour Al Génétique De Populations. 1996, Montpellier: Laboratoire Génome, Populations, Interactions.
112. Beerli P. Comparison of bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 2006, 22:341-345. 10.1093/bioinformatics/bti803, 16317072.
113. Hey J, Nielsen R. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 2004, 167:747-760. 10.1534/genetics.103.024182, 1470901, 15238526.
114. Hey J, Nielsen R. Integration within the Felsenstein equation for improved Markov Chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 2007, 104:2785-2790. 10.1073/pnas.0611164104, 1815259, 17301231.
115. Wirth T, Bernatchez L. Decline of North Atlantic eels: a fatal synergy?. Proc R Soc Lond B 2003, 270:681-688.