The Department of Biology, University of Maryland

Faculty A-Z

Dr. Thomas D. Kocher
Professor

Department of Biology
University of Maryland
College Park, MD 20742 USA
email: tdk@umd.edu
phone: (301) 405-4496

 

Evolution of African Cichlid Fishes

Introduction

In the lakes of East Africa, fishes of the family Cichlidae have undergone an extraordinarily rapid and extensive radiation. At least 1500 species of fish have arisen from a common ancestor in the last 10 million years. Within Lake Malawi over 700 species have arisen within just the last 2 MY. The overall objective of our research is to elucidate the evolutionary forces which have caused this rapid speciation. A number of factors are at work, including trophic specialization and sexual selection. We suspect that rapid evolution of male traits and female preferences contributes to pre-mating isolating mechanisms among local populations, facilitating speciation over small spatial scales. We are currently engaged in mapping genes for phenotypic traits associated with speciation, such as jaw morphology and adult color pattern. Our ultimate goal is to identify the genes responsible for speciation of these fishes, and to study the geographic distribution of allelic variants among populations and species in the wild.
  • Kocher TD. 2005. Fish models for studying adaptive evolution and speciation (Special Feature - Roundtable Discussion). Zebrafish 2(3): 147-156.(PDF)
  • Kocher TD. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288-298. (Abstract) (PDF)
  • Kocher TD, Albertson RC, Carleton KL and Streelman JT. 2002. The genetic basis of biodiversity: genomic studies of cichlid fishes. pp. 35-44 in Aquatic Genomics: Steps Toward a Great Future, N. Shimizu, T. Aoki, I. Hirono and F. Takashima, Editors. Springer, Tokyo. (PDF)
  • Danley PD and Kocher TD. 2001. Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology 10:1075-1086.(Abstract) (PDF)

Genetics and genomics

A key element of our approach to studying the diversification in these fishes is the development of genomic resources to support the identification of genes underlying the phenotypic differences among species. We published the first linkage map for a cichlid (tilapia) in 1998, and have since developed an extensive set of markers, maps and large insert DNA clone libraries. These resources are described on our Cichlid Genome Resources www page. Our genetic maps for East African species now include over 700 microsatellite markers, and we have developed physical maps based on the restriction fingerprints of more than 35,000 large-insert BAC clones.
  • DiPalma F, Kidd C, Borowsky R, Kocher TD. Construction of bacterial artificial chromosome libraries for two model fish species: the Lake Malawi cichlid (Metriaclima zebra), and the blind cavefish (Astyanax mexicanus). 2007. Zebrafish 4: (in press)(PDF)
  • Katagiri T, Kidd C. Tomasino E, Davis JT, Wishon C, Stern JE, Carleton KL, Howe AE, Kocher TD. 2005. A BAC-based physical map of the Nile tilapia genome. BMC Genomics 6:89. (PDF)
  • Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD. 2005. A second generation genetic linkage map of tilapia (Oreochromis spp.) Genetics 170: 237-244. (PDF)
  • Carleton, KL, Streelman JT, Lee BY, Garnhart N, Kidd M, and Kocher TD. 2002. Rapid isolation of CA microsatellites from the tilapia genome. Animal Genetics 33(2):140-4. (Abstract) (PDF)
  • Streelman JT and Kocher TD. 2000. From phenotype to genotype. Evolution and Development 2:166-173. (Abstract) (PDF)
  • Kocher TD, Lee WJ, Sobolewska H, Penman D and McAndrew B. 1998. A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148:1225-1232. (Abstract) (PDF)

Jaw and tooth morphology

East African cichlid fishes represent one of the most striking examples of rapid and convergent evolutionary radiation among vertebrates. Models of ecological speciation would suggest that functional divergence in feeding morphology has contributed to the origin and maintenance of cichlid species diversity. We have begun to explore the genetic basis of differences in cichlid oral jaw design. We first estimated the effective number of genetic factors controlling differences in the cichlid head through a comprehensive morphological assessment of two Lake Malawi cichlid species and their F1 and F2 hybrid progeny. We estimated that between one and 11 factors underlie shape difference of individual bony elements. A difference in tooth shape (bicuspid vs. tricuspid) appears to be controlled by a single major gene. We then went on to identify DNA markers linked to these genetic factors. Several chromosomal regions contain a disproportionate number of quantitative trait loci (QTL) indicating a prominent role for pleiotropy or genetic linkage in the divergence of this character complex. Our results imply that the rapid and replicative nature of cichlid trophic evolution is the result of directional selection on chromosomal packages that encode functionally linked aspects of the craniofacial skeleton.
  • Albertson RC, Kocher TD. 2006. Genetic and developmental basis of adaptive variation in the cichlid feeding apparatus. Heredity 97:211-221. (PDF)
  • Albertson RC, Streelman JT, Kocher TD, Yelick PC. 2005. Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proc. Natl. Acad. Sci. USA 102:16287-16292. (PDF)
  • Albertson RC, Kocher TD. 2005. Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution 59: 686-690. (PDF)
  • Streelman JT, Webb JF, Albertson RC and Kocher TD. 2003. The cusp of evolution and development: A model of cichlid tooth shape diversity. Evolution and Development 5: 600-608. (PDF)
  • Albertson RC, Streelman JT and Kocher TD. 2003. Genetic basis of adaptive shape differences in the cichlid head. J. Heredity 94(4):291-301. (Abstract) (PDF)
  • Albertson RC, Streelman JT and Kocher TD. 2003. Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc. Natl. Acad. Sci. USA 100: 5252-5257. (Abstract) (PDF)
  • Albertson RC and Kocher TD. 2001. Assessing morphological differences in an adaptive trait: a landmark-based morphometric approach. Journal of Experimental Zoology 289(6):385-403. (Abstract) (PDF)
  • Kocher TD, Conroy JA, McKaye KR and Stauffer JR. 1993. Similar morphologies of cichlids in lakes Tanganyika and Malawi are due to convergence. Molecular Phylogenetics and Evolution 2:158-165. (Abstract) (PDF)

Color patterns

Color pattern is a central feature of cichlid fish behavior and evolution. Hues from red to yellow to blue, in conjunction with stripes and bars, decorate cichlid bodies in a bewildering array of species-specific combinations. The brightest and gaudiest individuals are usually male. Cichlid colors are believed to confer mate recognition signals and are thought to evolve via sexual selection. Orange-blotch (OB) is a color pattern expressed mainly in females. It is sex-linked in several species, which caused Lande et al. to propose a model of speciation involving coevolution of color and the sex determining mechanism. We have used two different approaches to identify the region of the cichlid genome responsible for OB. We first used an interspecific cross to localize OB to a particular chromosomal region. We then used association mapping in a natural population to fine map the gene. Using comparative mapping data from the pufferfish (Takifugu rubripes) genome, we have identified positional candidate genes for this pigmentation phenotype.
  • Streelman JT, Albertson RC and Kocher TD. 2003. Genome mapping of the orange blotch color pattern in cichlid fishes. Molecular Ecology 12: 2465-2471. (Abstract) (PDF)

Breeding behavior

Malawi cichlids are maternal mouthbrooders. Females visit many males, and may lay eggs with several. The female picks the eggs up immediately after they are laid, and incubates them in her mouth for approximately three weeks until the fry have absorbed their yolk. Analysis of paternity using microsatellite DNA markers shows that individual females mate with several males in each spawning cycle. We are interested in identifying the characteristics females use to choose a mate, and the genetic basis of these female preferences. At least for some species, visual cues alone are sufficient to elicit species-specific mate preferences.
  • Kidd MR, Danley PD, Kocher TD. 2006. A direct assay of female choice in cichlid fishes: all the eggs in one basket. Journal of Fish Biology 68:373-384. (PDF)
  • Kidd MR, Kidd CE, Kocher TD. 2006. Axes of differentiaion in the bower building cichlids of Lake Malawi. Molecular Ecology 15: 459-478. (PDF)
  • Kellogg KA, Markert JA, Stauffer JR Jr. and Kocher TD. 1998. Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid. Behavioral Ecology 9(3): 309-312. (PDF)
  • Kellogg KA, Markert JA, Stauffer JR Jr and Kocher TD. 1995. Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proceedings Royal Society London Series B. 260:79-84. (PDF)
  • Kocher TD and McKaye KR. 1983. Territorial defense of heterospecific cichlids by Cyrtocara moorii in Lake Malawi, Africa. Copeia 1983:544-547. (PDF)
  • McKaye KR and Kocher T. 1983. Head ramming behavior by three paedophagous cichlids in Lake Malawi, Africa. Animal Behavior 31:206-210. (PDF)

Sex determination

The mechanisms of animal sex determination are diverse and highly labile. Even among species where sex is genetically (rather than environmentally) determined, different genes have been implicated as the primary regulators of sexual differentiation. Teleost fishes display a wonderful variety of mechanisms for sex determination and sex differentiation. Sexual differentiation of fishes is remarkably plastic, and is often controlled by both genetic and environmental factors. The sex chromosomes of African cichlids are still at an early stage of differentiation. There are no gross morphological differences in any chromosome pair, but a variety of evidence suggests that sex determination is principally monofactorial in most species. We have identified genetic markers linked to sex-determining genes in several species of cichlid. In the Nile tilapia (Oreochromis niloticus) we found microsatellite DNA markers tightly linked to an XY (male heterogametic system on linkage group 1. In O. aureus we identified markers consistent with a WZ on linkage group 3. Among the Lake Malawi cichlids we have found sex linkage on linkage groups 5 and 7. Our ultimate goals are to identify the genes underlying sex determination in this group of species, to reveal the molecular pathway of sex differentiation which they control, and to understand what role evolution of sex-determining mechanisms plays in speciation.
  • Cnaani A, Lee BY, Ozouf-Costaz C, Kocher TD. 2007 Mapping of Sox2 and Sox14 in tilapia (Oreochromis spp.). Sexual Development (in press).(PDF)
  • Lee BY, Kocher TD. Exclusion of Wilms Tumor (WT1_2) and ovarian aromatase (CYP19A1) as candidates for sex determining genes in Nile tilapia (Oreochromis niloticus). Animal Genetics 38: 85.(PDF)
  • Lee BY, Kocher TD. 2007. Comparative genomics and positional cloning. In J. Liu (ed.) Aquaculture Genome Technologies. Blackwell. (in press).(PDF)
  • Shirak A, Seroussi E, Cnaani A, Howe AE, Domokhovsky R, Zilberman N, Kocher TD, Hulata G, Ron M. 2006. Amh and Dmrta2 genes map to tilapia (Oreochromis spp.) linkage group 23 within QTL regions for sex determination. Genetics 174: 1573-1581. (PDF)
  • Lee B-Y, Hulata G, Kocher TD. 2004. Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity 92(6): 543-549. (PDF)
  • Lee B-Y, Penman, DJ and Kocher TD. 2003. Identification of a sex-determining region in Nile tilapia (Oreochromis niloticus) using bulked segregant analysis. Animal Genetics 34(5): 379-383. (PDF)

Population structure

Malawi cichlid populations are structured at extremely fine scales. The rock-dwelling species (mbuna) are so habitat-attached that a sandy beach ~100m long can cause a detectable decrease in gene flow. Nevertheless, levels of gene flow among nearby populations are typically large enough to prevent divergence by drift alone. Some form of selection is necessary to cause differentiation.
  • Streelman JT, Albertson RC, Kocher TD. Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology 52: 525-538. (PDF)
  • Danley PD, Markert JA, Arnegard ME, and Kocher TD. 2000. Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54(5):1725-37. (Abstract) (PDF)
  • Arnegard ME, Markert JA, Danley PD, Stauffer JR Jr., Ambali AJ and Kocher TD. 1999. Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed achipelago of rocky habitat patches in southern Lake Malawi. Proceedings Royal Society London B 266: 119-130. (PDF)
  • Markert, JA, Arnegard ME, Danley PD and Kocher TD. 1999. Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Mol. Ecol. 8(6): 1013-1026.(Abstract) (PDF)
  • Stauffer JR Jr, Bowers NJ, Kocher TD and McKaye KR. 1995. Hybridization between Cynotilapia afra and Pseudotropheus zebra (Teleostei: Cichlidae) following an intralacustrine introduction in Lake Malawi, Africa. Copeia 1996: 203-208. (PDF)
  • Bowers N, Stauffer JR, and Kocher TD. 1994. Intra- and interspecific mitochondrial DNA sequence variation within two species of rock-dwelling cichlids (Teleostei: Cichlidae) from Lake Malawi, Africa. Molecular Phylogenetics and Evolution 3:75-82. (Abstract) (PDF)
  • McKaye KR, Kocher T, Reinthal P, Harrison R and Kornfield I. 1984. Genetic evidence of allopatric and sympatric differentiation among color morphs of a Lake Malawi cichlid fish. Evolution 38:215-219. (PDF)
  • McKaye KR, Kocher T, Reinthal P, Harrison R and Kornfield I. 1982. A sympatric sibling species complex of Petrotilapia trewavas (Cichlidae) from Lake Malawi analyzed by enzyme electrophoresis. Zoological Journal of the Linnean Society 76:91-96. (PDF)

Phylogenetics

The patterns of phylogenetic relationships among fishes in different lakes are easily recovered from mitochondrial DNA sequences. Lake Tanganyika holds a group of 8-10 lineages that have been distinct for 7-9 million years. The independent monophyletic radiations in lakes Victoria and Malawi have occured in the last 1-2 million years. Morphologically similar species in different lakes are therefore the result of convergent evolution. Recovery of the phylogeny of species within lakes Victoria and Malawi is complicated by the retention of ancestral polymorphisms - speciation has occurred more rapidly than fixation of alleles within species. This means that that phylogenetic trees derived from particular genes may not accurately reflect the history of the species. To overcome this problem we have scored thousands of independent restriction site polymorphisms to produce a consensus that should accurately reflect the true history of species. These phylogenies are then used to test hypotheses about the mechanisms of speciation.
  • Kocher TD. 2003. Evolutionary biology: Fractious phylogenies (News and Views). Nature 423: 489 - 491. (PDF)
  • Albertson RC, Markert JA, Danley PD and Kocher TD. 1999. Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences USA 96(9): 5107-5110.(Abstract) (PDF)
  • Kocher TD, Conroy JA, McKaye KR, Stauffer JR and Lockwood SF. 1995. Evolution of the ND2 gene in East African cichlids. Molecular Phylogenetics and Evolution 4:420-432. (Abstract) (PDF)
  • Meyer A, Kocher TD and Wilson AC. 1992. African fishes. Nature 350:467-468. (PDF)
  • Meyer A, Kocher TD, Basaibwaki P and Wilson AC. 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550-553. (Abstract) (PDF)
  • Kornfield I, McKaye K and Kocher T. 1985. Evidence for the immigration hypothesis in the endemic cichlid fauna of Lake Tanganyika. Isozyme Bulletin 18:76. (PDF)

Crater lake cichlids

Cichlids inhabiting small volcanic crater lakes in Central America and Cameroon offer a simplified system within which to ecological speciation. We have contributed genetic evidence to support the conclusion that the small radiations of fishes within these lakes have arisen by sympatric speciation.

  • McKaye KR, Stauffer JR Jr, Van Den Berghe EP, Vivas R, Lopez Perez LJ, McCrary JK, Waid R, Konings A, Lee WJ and Kocher TD. 2002. Behavioral, Morphological and Genetic Evidence of Divergence of the Midas Cichlid Species Complex in Two Nicaraguan Crater Lakes. Cuadernos de la Investigacion de la UCA, volume 12; p 19-47. (PDF)
  • Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T and Tautz D. 2001. Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Molecular Ecology 10(6):1471-1488. (Abstract) (PDF)
  • Stauffer JR Jr, Bowers NJ, McKaye KR and Kocher TD. 1995. Evolutionary significant units among cichlid fishes: the role of behavioral studies. American Fisheries Society Symposia 17: 227-244. (PDF)
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