Advertisement

Reviews in Fish Biology and Fisheries

, Volume 20, Issue 2, pp 187–202 | Cite as

Species concepts, speciation, and taxonomic change in the Lake Malawi mbuna, with special reference to the genus Labeotropheus Ahl 1927 (Perciformes: Cichlidae)

Article

Abstract

While the debate over species concepts and criteria affects all organisms on Earth, no group of organisms demonstrates a need for a consilient, universal species concept better than the haplochromine cichlids of Lake Malawi. These fishes, which are the single greatest radiation of vertebrates on the planet, are a daunting taxonomic puzzle for ichthyologists and evolutionary biologists who try to piece together the history and diversity of these fishes. Accordingly, a number of attempts to apply species concepts to these fishes have been attempted, though rarely with a satisfactory outcome. Focusing on the rock-dwelling cichlids, or mbuna, of Lake Malawi, I evaluate the species concepts that have been applied to these fishes, and conclude that the consilient formulation of the Evolutionary Species Concept is the most appropriate species concept to apply to both our current understanding of the mbuna, and future investigations of mbuna speciation and taxonomy. To further demonstrate the applicability and utility of the Evolutionary Species Concept, I provide a closer examination of the genus Labeotropheus, which has been overlooked in recent taxonomic investigations of the mbuna. While most other mbuna genera have had additional, formally described species added to them, if not additional provisionally named species, Labeotropheus has been ignored, largely due to inappropriately applied species concepts and criteria. I provide a possible research program for the Labeotropheus, based on the consilient formulation of the Evolutionary Species Concept, culminating in the description of new species.

Keywords

Lake Malawi Speciation Adaptive radiation Species concepts Evolutionary species concept Allopatry Taxonomy Labeotropheus 

Notes

Acknowledgments

This work was supported by an American Cichlid Association Guy D. Jordan Fellowship, the Milwaukee County Zoological Society, and the Clifford Mortimer and Ruth Walker funds of the University of Wisconsin-Milwaukee. Postdoctoral support was provided by Jay and Maureen Neitz during the preparation of this manuscript. Ad Konings graciously provided almost all of the images of Labeotropheus (except for L. fuelleborni Katale) and the map used in Fig. 1. Discussions with Harvey Bootsma, Tim Ehlinger, Randy Mooi, and Jeff McKinnon inspired and improved the ideas presented herein. Joshua M. Kapfer and Craig S. Berg commented on the manuscript during various stages of its preparation, and made several helpful suggestions. The final version of the manuscript was greatly improved due to the comments and input of an anonymous reviewer. I am indebted to my amazing wife, Montine R. Pauers, for her financial and emotional support during the finalization of this manuscript.

References

  1. Adams B (2001) The species delimitation uncertainty principle. J Nematol 33(4):153–160PubMedGoogle Scholar
  2. Ahl E (1927) Einge neue Fische der Famile Cichlidae aus dem Nyassa-see. Schrift Berlin Gesellschaft Natur Freunde Berl 1926:51–62Google Scholar
  3. Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, east Africa. PNAS (USA) 96:5107–5110CrossRefGoogle Scholar
  4. Arnegard ME, Markert JA, Danley PD, Stauffer JR, Ambali AJ, Kocher TD (1999) Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proc Roy Soc Lond B 266:119–130CrossRefGoogle Scholar
  5. Barlow GW (2000) The Cichlid fishes: nature’s grand experiment in evolution. Perseus Press, CambridgeGoogle Scholar
  6. Barlow GW (2002) How behavioural studies contribute to the species problem: a piscine perspective. Fish Fish 3:197–212Google Scholar
  7. Blais J, Plenderleith M, Rico C, Taylor MI, Seehausen O, van Ooseterhout C, Turner GF (2009) Assortative mating among Lake Malawi cichlid fish populations is not simply predictable from male nuptial colour. BMC Evol Biol 9:53CrossRefPubMedGoogle Scholar
  8. Boughman J (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948CrossRefPubMedGoogle Scholar
  9. Carleton KL, Kocher TD (2001) Cone opsin genes of African cichlid fishes: tuning spectral sensitivity by differential gene expression. Mol Biol Evol 18(8):1540–1550PubMedGoogle Scholar
  10. Carleton KL, Hárosi FI, Kocher TD (2000) Visual pigments of African cichlid fishes: evidence for ultraviolet vision from microspectrophotometry and DNA sequences. Vis Res 40(8):879–890CrossRefPubMedGoogle Scholar
  11. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  12. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 57–75Google Scholar
  13. de Queiroz K (2005) Ernst Mayr and the modern concept of species. PNAS (USA) 102(suppl. 1):6600–6607CrossRefGoogle Scholar
  14. Dominey WJ (1984) Effects of sexual selection and life-history in speciation: species flocks in African cichlids and Hawaiian Drosophila. In: Echelle AA, Kornfield I (eds) The evolution of species flocks. University of Maine Press, Orono, pp 231–249Google Scholar
  15. Fryer G (1956) A new species of Labeotropheus from Lake Nyasa, with a redescription of Labeotropheus fuelleborni Ahl and some notes on the genus Labeotropheus (Pisces: Cichlidae). Rev Zool Bot Afr 54:280–289Google Scholar
  16. Fryer G (1959) The trophic interrelationships and ecology of some littoral communities in Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proc Zool Soc Lond 132:153–281Google Scholar
  17. Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa. Oliver & Boyd, EdinburghGoogle Scholar
  18. Genner MJ, Turner GF (2005) The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish Fish 6:1–34Google Scholar
  19. Genner MJ, Taylor MI, Cleary DFR, Hawkins SJ, Knight ME, Turner GF (2004a) Beta diversity of rock-restricted cichlid fishes in Lake Malawi: importance of environmental and spatial factors. Ecography 27:601–610CrossRefGoogle Scholar
  20. Genner MJ, Seehausen O, Cleary DFR, Knight ME, Michel E, Turner GF (2004b) How does the taxonomic status of allopatric populations influence species richness within African cichlid fish assemblages? J Biogeogr 31:93–102Google Scholar
  21. Gill AC (1999) Subspecies, geographic forms and widespread Indo-Pacific coral-reef fish species: a call for change in taxonomic practice. In: Séret B, Sire J-Y (eds) Proceedings of the fifth Indo-Pacific fish conference (Nouméa 1997). French Society of Ichthyologists, Paris, pp 79–87Google Scholar
  22. Greenwood PH (1974) The cichlid fishes of Lake Victoria, East Africa: the biology and evolution of a species flock. Bull Br Mus Nat Hist (Zool) (Suppl 6): 1–134Google Scholar
  23. Greenwood PH (1991) Speciation. In: Keenleyside MHA (ed) Cichlid fishes: behaviour, ecology and evolution. Chapman & Hall, London, pp 86–102Google Scholar
  24. Hey J, Waples RS, Arnold ML, Butlin RK, Harrison RG (2003) Understanding and confronting species uncertainty in biology and conservation. TREE 18(11):597–603Google Scholar
  25. Jacobs GH (1981) Comparative color vision. Academic Press, New YorkGoogle Scholar
  26. Jordan RC, Kellogg K, Juanes F, Stauffer JR Jr (2003) Evaluation of female mate choice cues in a group of Lake Malawi mbuna. Copeia 2003:181–186CrossRefGoogle Scholar
  27. Knight ME, Turner GF (2004) Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi. Proc Roy Soc Lond B 271(1540):675–680CrossRefGoogle Scholar
  28. Konings A (2007a) Protecting Malawi cichlids. Buntbarsche Bull 2007(243):4–10Google Scholar
  29. Konings A (2007b) Malawi Cichlids in their natural habitat, 4th edn. Cichlid Press, El PasoGoogle Scholar
  30. 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 T, Stepien C (eds) Molecular systematics of fishes. Academic Press, San Diego, pp 25–37CrossRefGoogle Scholar
  31. Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196CrossRefGoogle Scholar
  32. Lewis DSC (1982) Problems of species definition in Lake Malawi cichlid fishes (Pisces: Cichlidae). Spec Publ J LB Smith Inst Ichthyol 23:1–5Google Scholar
  33. Maan ME, Hofker KD, van Alphen JJ, Seehausen O (2006) Sensory drive in cichlid speciation. Am Nat 167(6):947–954CrossRefGoogle Scholar
  34. Mallett J (1995) A species definition for the modern synthesis. Trends Ecol Evol 10:294–299CrossRefGoogle Scholar
  35. Mayden RL (1999) Consilience and a hierarchy of species concepts: advances toward closure on the species puzzle. J Nematol 31(2):95–116PubMedGoogle Scholar
  36. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  37. Mayr E (1995) Species, classification, and evolution. In: Arai R, Kato M, Doi Y (eds) Biodiversity and evolution. National Science Museum Foundation, Tokyo, pp 3–12Google Scholar
  38. Mayr E (2000) The biological species concept. In: Wheeler QD, Meier M (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 17–29Google Scholar
  39. McElroy DM, Kornfield I (1990) Sexual selection, reproductive behavior, and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae). Environ Biol Fish 28:273–284CrossRefGoogle Scholar
  40. McKaye KR, Kocher T, Reinthal P, Harrison R, Kornfield I (1984) Genetic evidence for allopatric and sympatric differentiation among morphs of a Lake Malawi cichlid fish. Evolution Int J org Evolution 38:215–219Google Scholar
  41. Mishler BD (1999) Getting rid of species? In: Wilson RA (ed) Species: new interdisciplinary essays. MIT Press, Cambridge, pp 307–315Google Scholar
  42. Muntz WRA (1976) Visual pigments of cichlid fishes from Malawi. Vis Res 16:897–903CrossRefPubMedGoogle Scholar
  43. Nshombo M (1994) Polychromatism of the scale-eater Perissodus microlepis (Cichlidae, Teleostei) in relation to foraging behavior. J Ethol 12:141–161Google Scholar
  44. Paterson HEH (1978) More evidence against speciation by reinforcement. S Afr J Sci 74:369–371Google Scholar
  45. Paterson HEH (1985) The recognition concept of species. In: Vrba ES (ed) Species and speciation. Transvaal Museum Press, Pretoria, pp 21–29Google Scholar
  46. Paterson HEH (1993) Evolution and the recognition concept of species. Johns Hopkins University Press, BaltimoreGoogle Scholar
  47. Pauers MJ (2004) Naturally and sexually selected constraints on morphology, behavior, and coloration in the African cichlid genus Labeotropheus. Unpublished Ph.D. Dissertation, The University of Wisconsin-MilwaukeeGoogle Scholar
  48. Pauers MJ, McKinnon JS, Ehlinger TJ (2004) Directional sexual selection on chroma and within-pattern contrast in Labeotropheus fuelleborni. Proc Roy Soc Lond B (Suppl) 271:S444–S447CrossRefGoogle Scholar
  49. Pauers MJ, Kapfer JM, Fendos CE, Berg CS (2008) Aggressive biases towards similarly coloured males in Lake Malawi cichlid fishes. Biol Lett 4(2):156–159CrossRefPubMedGoogle Scholar
  50. Pauers MJ, Ehlinger TJ, McKinnon JS (2009) Female and male visually-based mate preferences are consistent with reproductive isolation between populations of the Lake Malawi endemic Labeotropheus fuelleborni. Curr Zool (in press)Google Scholar
  51. Ribbink AJ (1986) The species concept, sibling species and speciation. Ann Musée roy l’Afr Centr, Sci Zool 251:109–116Google Scholar
  52. Ribbink AJ (1994) Alternative perspectives on some controversial aspects of cichlid fish speciation. Arch Hydrobiol 44:101–125Google Scholar
  53. Ribbink AJ, Marsh BA, Marsh AC, Ribbink AC, Sharp BJ (1983a) A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. S Afr J Zool 18:149–310Google Scholar
  54. Ribbink AJ, Marsh AC, Marsh BA, Sharp BJ (1983b) The zoogeography, ecology, taxonomy of the genus Labeotropheus Ahl, 1927 of Lake Malawi (Pisces: Cichlidae). Zool J Linn Soc 79:223–243CrossRefGoogle Scholar
  55. Rico C, Turner GF (2002) Extreme microallopatric divergence in a cichlid species from Lake Malawi. Mol Ecol 11(8):1585–1590CrossRefPubMedGoogle Scholar
  56. Rico C, Bouteillon P, van Oppen MJH, Knight ME, Hewitt GM, Turner GF (2003) No evidence for parallel sympatric speciation in cichlid species of the genus Pseudotropheus from north-western Lake Malawi. J Evol Biol 16(1):37–46CrossRefPubMedGoogle Scholar
  57. Seehausen O, Schlüter D (2004) Male–male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc Roy Soc (Lond) B 271(1546):1345–1353CrossRefGoogle Scholar
  58. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–627CrossRefPubMedGoogle Scholar
  59. Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New YorkGoogle Scholar
  60. Snoeks J (2000) How well known is the ichthyodiversity of the ancient African lakes? In: Rossiter A, Kawanabe H (eds) Ancient lakes: biodiversity, ecology and evolution: advances in ecological research 31. Academic Press, London, pp 17–38CrossRefGoogle Scholar
  61. Snoeks J, Ruber L, Verheyen E (1994) The Tanganyika problem: comments on the taxonomy and distribution patterns of its cichlid fauna. Arch Hydrobiol 44:355–372Google Scholar
  62. Spady TC, Seehausen O, Loew ER, Jordan RC, Kocher TD, Carleton KL (2005) Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Mol Biol Evol 22:1412–1422CrossRefPubMedGoogle Scholar
  63. Spencer HG, Lambert DM, McArdle BH (1987) Reinforcement, species, and speciation: a reply to Butlin. Am Nat 130:958–962Google Scholar
  64. Stauffer JR Jr, Konings AF (2006) Review of Copadichromis (Teleostei: Cichlidae) with the description of a new genus and six new species. Ichthyol Explor Freshw 17(1):9–42Google Scholar
  65. Stauffer JR Jr, Bowers NJ, Kocher TD, McKaye KR (1996) Evidence of hybridization between Cynotilapia afra and Pseudotropheus zebra (Teleostei: Cichlidae) following an intralacustrine translocation in Lake Malawi. Copeia 1996(1):203–208CrossRefGoogle Scholar
  66. Stauffer JR Jr, Bowers NJ, Kellogg KA, McKaye KR (1997) A revision of the blue-black Pseudotropheus zebra (Teleostei: Cichlidae) complex from Lake Malawi, Africa, with a description of a new genus and ten new species. Proc Acad Nat Sci Phila 148:189–230Google Scholar
  67. Stauffer JR Jr, McKaye KR, Konings AF (2002) Behaviour: an important diagnostic tool for Lake Malawi cichlids. Fish Fish 3:213–224Google Scholar
  68. Trewavas E (1935) A synopsis of the cichlid fishes of Lake Nyasa. Ann Mag Nat Hist 10(16):65–118Google Scholar
  69. Turner GF (1994) Speciation in Lake Malawi cichlids: a critical review. Arch Hydrobiol 44:139–160Google Scholar
  70. Turner GF (1999) What is a fish species? Rev Fish Biol Fisheries 9(4):281–297CrossRefGoogle Scholar
  71. Turner GF (2000) The nature of species in ancient lakes: perspectives from the fishes of Lake Malawi. Adv Ecol Res 31:39–60CrossRefGoogle Scholar
  72. Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Mol Ecol 10:793–806CrossRefPubMedGoogle Scholar
  73. van Oppen MJH, Turner GF, Rico C, Deutsch JC, Ibrahim KM, Robinson RL, Hewitt GM (1997) Unusually fine-scale genetic structuring found in rapidly speciating Malawi cichlid fishes. Proc Roy Soc B 264(1389):1803–1812CrossRefGoogle Scholar
  74. van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25:233–239CrossRefGoogle Scholar
  75. Wiens JJ (2004a) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution Int J org Evolution 58:193–197Google Scholar
  76. Wiens JJ (2004b) What is speciation and how should we study it? Am Nat 163:914–923CrossRefPubMedGoogle Scholar
  77. Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26CrossRefGoogle Scholar
  78. Wiley EO, Mayden RD (2000) The evolutionary species concept. In: Wheeler QD, Meier M (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 70–89Google Scholar
  79. Willmann R, Meier R (2000) A critique from the Hennigian species concept perspective. In: Wheeler QD, Meier M (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 101–118Google Scholar
  80. Wilson EO (1992) The diversity of life. National Academy of Science Press, CambridgeGoogle Scholar
  81. Young KA, Whitman JM, Turner GF (2009) Secondary contact during adaptive radiation: a community matrix for Lake Malawi cichlids. J Evol Biol 22(4):882–889CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Division of Natural and Health SciencesCarroll UniversityWaukeshaUSA

Personalised recommendations