Advertisement

Journal of Molecular Evolution

, Volume 45, Issue 1, pp 70–83 | Cite as

Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of lake Malawi, East Africa

  • Alex Parker
  • Irv Kornfield
Article

Abstract

Considerable controversy has surrounded the application of mitochondrial DNA data to reconstruction of evolutionary relationships among the endemic cichlids of Lake Malawi. Central to this debate has been the issue of whether lineage sorting is complete, and thus whether these data actually reflect species phylogeny, or simply gene genealogy. Review of all mtDNA control region sequences available for members of one monophyletic subset of this species flock, the Malawi rockfishes, or mbuna, strongly indicates that lineage sorting is incomplete: Character-based analyses of these sequences reconstruct gene, not species, interrelationships. Analysis of the pattern of nucleotide substitutions differentiating these mtDNA alleles suggests that pyrimidine residues undergo transition substitutions more often than do purines. Estimation of the magnitude of derived sequence differentiation in light of the reconstructed gene genealogy suggests that the mbuna may be of considerably more recent vintage than previous molecular characterizations have indicated.

Key words

mbuna species Lake Malawi Mitochondrial DNA control region 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New YorkGoogle Scholar
  2. Bowers N, Stauffer JR, Kocher TD (1994) Intra- and interspecific mitochondrial DNA sequence variation within two species of rock-dwelling cichlids (Teleostei: Cichlidae) from Lake Malawi, Africa. Mol Phyl Evol 3:75–82CrossRefGoogle Scholar
  3. Brown GG, Prager EM, Wang A, Wilson AC (1986) Structural conservation and variation in the d-loop containing region of vertebrate mitochondrial DNA. J Mol Biol 192:503–511PubMedCrossRefGoogle Scholar
  4. Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci 5:233–234PubMedGoogle Scholar
  5. Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Syst 15:97–131CrossRefGoogle Scholar
  6. Collins TM, Kraus F, Estabrook G (1994) Compositional effects and weighting of nucleotide sequences for phylogenetic analysis. Syst Biol 43:449–459Google Scholar
  7. Dominey WJ (1984) Effects of sexual selection and life history on speciation: Species flocks in African cichlids and Hawaiian Drosophila. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine Press, Orono, pp 231–250Google Scholar
  8. Eccles DH, Trewavas E (1989) Malawian cichlid fishes: the classification of some haplochromine genera Lake Fish. Movies Herten, West GermanyGoogle Scholar
  9. Echelle AA, Kornfield I (eds) (1984) Evolution of fish species flocks. University of Maine Press, OronoGoogle Scholar
  10. Fryer G (1959) The trophic interrelationships and ecology of some littoral communities in Lake Nyasa with special references to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proc. Zool Soc Lond 132:153–281Google Scholar
  11. Fryer G, Iles TD (1972) The cichlid fishes of the great lakes of Africa. Oliver Boyd, EdinboroughGoogle Scholar
  12. Futuyma D (1986) Evolutionary biology. Sinauer, Sunderland, MAGoogle Scholar
  13. Greenwood PH (1984) African cichlids and evolutionary theories. In: Echelle AA, Kornfield IL (eds) Evolution of fish species flocks. University of Maine Press, Orono, pp 141–154Google Scholar
  14. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86:958–962PubMedCrossRefGoogle Scholar
  15. Keenlyside M (ed) (1991) Cichlid fishes: behavior, ecology, and evolution. Chapman and Hall, LondonGoogle Scholar
  16. Kellogg KA, Markert JA, Stauffer JR, Kocher TD (1995) Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proc R Soc Lond [Biol] 260B:79–84CrossRefGoogle Scholar
  17. Kimura M, Ohta T (1969) The average number of generations until fixation of an individual mutant gene in a finite population. Genetics 61:763–771PubMedGoogle Scholar
  18. Kocher TD, Conroy JA, McKaye KR, Stauffer JR (1993) Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol Phyl Evol 2:158–165CrossRefGoogle Scholar
  19. Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF (1995) Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Mol Phyl Evol 4:420–432CrossRefGoogle Scholar
  20. Konings A (1990) Konings’ book of cichlids and all the other fishes of Lake Malawi. TFH, Neptune City, NJGoogle Scholar
  21. Kornfield I (1978) Evidence for rapid speciation in African cichlid fishes. Experientia 34:335–336CrossRefGoogle Scholar
  22. Kornfield I (1991) Genetics. In: Keenlyside MHA (ed) Cichlid fishes: behavior, ecology and evolution. Chapman and Hall, London, pp 103–128Google Scholar
  23. Kornfield I, Parker A (1997) Molecular systematics of a rapidly evolving species flock: the mbuna of Lake Malawi and the search for phylogenetic signal. In: Kocher TD, Stepien C (eds) Molecular systematics of fishes. Academic Press, New York, pp 25–37CrossRefGoogle Scholar
  24. Kosswig C (1947) Selective mating as a factor for speciation in cichlid fish of East African lakes. Nature 159:604–605CrossRefGoogle Scholar
  25. Kosswig C (1963) Ways of speciation in fishes. Copeia 1963:238–244CrossRefGoogle Scholar
  26. Lee WJ, Conroy J, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–65PubMedCrossRefGoogle Scholar
  27. Lehman N, Pfrender ME, Morin PA, Crease TJ, Lynch M (1995) A hierarchical molecular phylogeny within the genus Daphnia. Mol Phyl Evol 4:395–407CrossRefGoogle Scholar
  28. Lewis D, Reinthal P, Trendall J (1986) A guide to the fishes of Lake Malawi National Park. World Wildlife Fund Publications, Gland, SwitzerlandGoogle Scholar
  29. Lyrholm T, Leimar O, Gyllensten U (1996) Low diversity and biased substitution patterns in the mitochondrial DNA control region of sperm whales: implications for estimates of time since common ancestry. Mol Biol Evol 13:1318–1326PubMedGoogle Scholar
  30. Martin A (1995) Mitochondrial DNA sequence evolution in sharks: rates, patterns, and phylogenetic inferences. Mol Biol Evol 12:1114–1123PubMedGoogle Scholar
  31. Mayr E (1984) Evolution of fish species flocks: a commentary. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine Press, Orono, pp 3–12Google Scholar
  32. McElroy DM, Kornfield I (1990) Sexual selection, reproductive behavior, and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae). Env Biol Fishes 28:273–284CrossRefGoogle Scholar
  33. McKaye KR (1991) Sexual selection and the evolution of the cichlid fishes of Lake Malawi, Africa. In: Keenlyside MHA (ed) Cichlid fishes: behavior, ecology and evolution. Chapman and Hall, London, pp 241–257Google Scholar
  34. McKaye KR, Gray WN (1984) Extrinsic barriers to gene flow in rock dwelling cichlids of Lake Malawi: microhabitat heterogeneity and reef colonization. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine Press, Orono, pp 169–184Google Scholar
  35. McKaye KR, Kocher T, Reinthal P, Kornfield I (1982) Sympatric sibling species complex of Petrotilapia Trewavas analysed by enzyme electrophoresis (Pisces: Cichlidae). J Linn Soc 76:91–96CrossRefGoogle Scholar
  36. McKaye KR, Kocher TD, Reinthal P, Harrison R, Kornfield I (1984) Genetic evidence for allopatric and sympatric differentiation among morphs of a Lake Malawi cichlid fish. Evolution 38:215–219CrossRefGoogle Scholar
  37. Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 8:279–284CrossRefGoogle Scholar
  38. Meyer A, Kocher TD, Bassaslowski P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553PubMedCrossRefGoogle Scholar
  39. Moran P, Kornfield I (1993) Retention of an ancestral polymorphism in the mbuna species flock (Pisces: Cichlidae) of Lake Malawi. Mol Biol Evol 10:1015–1029Google Scholar
  40. Moran P, Kornfield I (1995) Evidence of a population bottleneck and extreme philopatry in the mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol Biol Evol 12:1085–1093Google Scholar
  41. Moran P, Kornfield I, Reinthal P (1994) Molecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake Malawi. Copeia 1994:274–288CrossRefGoogle Scholar
  42. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  43. Owen RB, Crossley R, Johnson TC, Tweddle D, Kornfield I, Davison S, Eccles DH, Engstrom DE (1990) Major low levels of Lake Malawi and implication for speciation rates in cichlid fishes. Proc R Soc Lond [Biol] 240B:519–553CrossRefGoogle Scholar
  44. Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583PubMedGoogle Scholar
  45. Parker A, Kornfield I (1995) A molecular perspective on evolution and zoogeography of cyprinodontid killifishes. Copeia 1995:8–21.CrossRefGoogle Scholar
  46. Parker A, Kornfield I (1996a) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi, Africa. Env Biol Fishes 47:345–352CrossRefGoogle Scholar
  47. Parker A, Kornfield I (1996b) An improved amplification and sequencing strategy for phylogenetic studies using the mitochondrial large subunit ribosomal RNA. Genome 39:793–797PubMedCrossRefGoogle Scholar
  48. Patterson HE (1980) A comment of mate recognition systems. Evolution 34:330–331CrossRefGoogle Scholar
  49. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358PubMedCrossRefGoogle Scholar
  50. Rand DM, Dorfsman M, Kan LM (1994) Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics 138:741–756PubMedGoogle Scholar
  51. Reinthal PN (1987) Morphology, ecology, and behavior of a group of the rock-dwelling fishes (Cichlidae: Perciformes) from Lake Malawi, Africa. Unpublished PhD dissertation, Duke University, DurhamGoogle Scholar
  52. Reinthal PN (1990) The living jewels of Lake Malawi. Natl Geogr 177:42–51Google Scholar
  53. Reinthal PN, Meyer A (1997) Genetic tests of speciation models in African cichlid fishes. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiations. Cambridge University Press, Cambridge (in press)Google Scholar
  54. Ribbink AJ, Marsh BA, Marsh AC, Ribbink AC, Sharp BJ (1983) A preliminary survey of the cichlid fishes of the rocky habitats in Lake Malawi. S Afr J Sci 18:149–310Google Scholar
  55. Ricklefs RE, Schluter D (1993) Species diversity: regional and historical influences. In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities. University of Chicago Press, Chicago, pp 350–363Google Scholar
  56. Ruvolo M (1996) A new approach to studying modern human origins: hypothesis testing with coalescence time distributions. Mol Phyl Evol 5:202–219CrossRefGoogle Scholar
  57. Sage D, Seiander RK (1975) Trophic radiation through polymorphism in cichlid fishes. Proc Natl Acad Sci 72:4669–4673PubMedCrossRefGoogle Scholar
  58. Shields GF, Kocher TD (1991) Phylogenetic relationships of North American ursids based on analysis of mitochondrial DNA. Evolution 45:218–221CrossRefGoogle Scholar
  59. Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155PubMedGoogle Scholar
  60. Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, ver 3.1.1. Computer program distributed by the Illinois Natural History Survey, Champaign, ILGoogle Scholar
  61. 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 10:512–526PubMedGoogle Scholar
  62. Templeton AR (1993) The “Eve” hypothesis: a genetic critique and reanalysis. Am Anthropol 95:51–72CrossRefGoogle Scholar
  63. Templeton AR (1996) Contingency tests of neutrality using intra/ interspecific gene trees: the rejection of neutrality for the evolution of the mitochondrial cytochrome oxidase II gene in the hominid primates. Genetics 144:1263–1270PubMedGoogle Scholar
  64. Trewavas E (1935) A synopsis of the cichlid fishes of Lake Nyasa. Ann Mag Nat Hist 10:65–118Google Scholar
  65. Turner GF (1994) Speciation mechanisms in Lake Malawi cichlids: a critical review. Arch Hydrobiol 44:139–160Google Scholar
  66. Wakeley J (1993) Substitution rate variation among sites in hypervariable region I of human mitochondrial DNA. J Mol Evol 37:613–623PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1997

Authors and Affiliations

  • Alex Parker
    • 1
  • Irv Kornfield
    • 1
  1. 1.Department of ZoologyUniversity of MaineOronoUSA

Personalised recommendations