Genetic basis of adaptive shape differences in the cichlid head.

East African cichlids exhibit an extraordinary level of morphological diversity. Key to their success has been a dramatic radiation in trophic biology, which has occurred rapidly and repeatedly in different lakes. In this report we take the first step in understanding the genetic basis of differences in cichlid oral jaw design. We estimate the effective number of genetic factors that control differences in the cichlid head through a comprehensive morphological assessment of two Lake Malawi cichlid species and their F(1) and F(2) hybrid progeny. We estimate that between one and 11 factors underlie shape difference of individual bony elements. We show that many of the skeletal differences in the head and oral jaw apparatus are inherited together, suggesting a degree of pleiotropy in the genetic architecture of this character complex. Moreover, we find that cosegregation of shape differences in different elements corresponds to developmental, rather than functional, units.

[1]  K. R. Mckaye,et al.  Food switching by two specialized algae-scraping cichlid fishes in Lake Malawi, Africa , 1983, Oecologia.

[2]  Katsu Takahashi,et al.  Positionally‐dependent chondrogenesis induced by BMP4 is co‐regulated by sox9 and msx2 , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[3]  J. Mcphail Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia , 1992 .

[4]  R. C. Albertson Genetic basis of adaptive radiation in East African cichlids , 2002 .

[5]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[6]  F. Rohlf,et al.  Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A. Meyer Phylogenetic relationships and evolutionary processes in East African cichlid fishes. , 1993, Trends in ecology & evolution.

[8]  R. Balling,et al.  Teeth. Where and how to make them. , 1999, Trends in genetics : TIG.

[9]  P. Sharpe,et al.  Transformation of tooth type induced by inhibition of BMP signaling. , 1998, Science.

[10]  D. Noakes,et al.  Ontogeny of trophic morphology in four sympatric morphs of arctic charr Salvelinus alpinus in Thingvallavatn, Iceland , 1989 .

[11]  K. Liem Adaptive Significance of Intra- and Interspecific Differences in the Feeding Repertoires of Cichlid Fishes , 1980 .

[12]  I. Kornfield,et al.  Major low levels of Lake Malawi and their implications for speciation rates in cichlid fishes , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[13]  C. Cockerham,et al.  How informative is Wright's estimator of the number of genes affecting a quantitative character? , 1990, Genetics.

[14]  Z. Zeng,et al.  Correcting the bias of Wright's estimates of the number of genes affecting a quantitative character: a further improved method. , 1992, Genetics.

[15]  G. Martin,et al.  The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. , 1995, Development.

[16]  P. Reinthal The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi, Africa , 1990, Environmental Biology of Fishes.

[17]  J. Cheverud 18 – The Genetic Architecture of Pleiotropic Relations and Differential Epistasis , 2001 .

[18]  J. Cheverud,et al.  Quantitative Trait Loci for Early‐ and Late‐Developing Skull Characters in Mice: A Test of the Genetic Independence Model of Morphological Integration , 1999, The American Naturalist.

[19]  G. P. Wagner,et al.  Is the genotype-phenotype map modular? A statistical approach using mouse quantitative trait loci data. , 2000, Genetics.

[20]  S. Leal Genetics and Analysis of Quantitative Traits , 2001 .

[21]  D'arcy W. Thompson On Growth and Form , 1945 .

[22]  J. Cheverud PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM , 1982, Evolution; international journal of organic evolution.

[23]  John Doebley,et al.  MORPHOLOGICAL TRAITS DEFINING SPECIES DIFFERENCES IN WILD RELATIVES OF MAIZE ARE CONTROLLED BY MULTIPLE QUANTITATIVE TRAIT LOCI , 2002, Evolution; international journal of organic evolution.

[24]  T. Kocher,et al.  Assessing morphological differences in an adaptive trait: a landmark-based morphometric approach. , 2001, The Journal of experimental zoology.

[25]  R. Maas,et al.  Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development , 1994, Nature Genetics.

[26]  D A Kane,et al.  Jaw and branchial arch mutants in zebrafish I: branchial arches. , 1996, Development.

[27]  B. J. Sharp,et al.  A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi , 1983 .

[28]  C. Kimmel,et al.  Specification and morphogenesis of the zebrafish larval head skeleton. , 2001, Developmental biology.

[29]  C. Nüsslein-Volhard,et al.  Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. , 1996, Development.

[30]  P. Brakefield,et al.  The genetic basis of eyespot size in the butterfly Bicyclus anynana: an analysis of line crosses , 2000, Heredity.

[31]  E. Lammens,et al.  The barbs (Barbus spp.) of Lake Tana: a forgotten species flock? , 2004, Environmental Biology of Fishes.

[32]  E. Bermingham,et al.  Systematics and evolution of lower Central American cichlids inferred from analysis of cytochrome b gene sequences. , 1998, Molecular phylogenetics and evolution.

[33]  M. Zelditch Evaluating Models of Developmental Integration in the Laboratory Rat Using Confirmatory Factor Analysis , 1987 .

[34]  I. Kornfield,et al.  Novel jaw morphology in hybrids between Pseudotropheus zebra and Labeotropheus fuelleborni (Teleostei: Cichlidae) from Lake Malawi, Africa , 1993 .

[35]  S. Boissinot,et al.  Evolutionary Biology , 2000, Evolutionary Biology.

[36]  Corbin D. Jones,et al.  Detecting the undetected: estimating the total number of loci underlying a quantitative trait. , 2000, Genetics.

[37]  T. Kocher,et al.  Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Rubenstein,et al.  Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. , 1997, Developmental biology.

[39]  Fred L. Bookstein,et al.  Principal Warps: Thin-Plate Splines and the Decomposition of Deformations , 1989, IEEE Trans. Pattern Anal. Mach. Intell..

[40]  Lucia Allen Yaroch,et al.  Shape analysis using the thin‐plate spline: Neanderthal cranial shape as an example , 1996 .

[41]  T. Hatfield,et al.  Genetic Divergence in Adaptive Characters Between Sympatric Species of Stickleback , 1997, The American Naturalist.

[42]  K. Kratochwil,et al.  Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. , 1998, Genes & development.

[43]  B. Grant,et al.  On the origin of Darwin's finches. , 2001, Molecular biology and evolution.

[44]  A. Lumsden,et al.  Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. , 1996, Development.

[45]  H. A. Orr,et al.  The Genetics of Adaptation: A Reassessment , 1992, The American Naturalist.

[46]  W. Beavis QTL Analyses: Power, Precision, and Accuracy , 1997, Molecular Dissection of Complex Traits.

[47]  M. Depew,et al.  Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. , 1999, Genes & development.

[48]  Peter Humphrey Greenwood,et al.  The cichlid fishes of Lake Victoria, East Africa: The biology and evolution of a species flock. , 1974 .

[49]  D. Tautz,et al.  Sympatric speciation suggested by monophyly of crater lake cichlids , 1994, Nature.

[50]  Karel F. Liem,et al.  Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws , 1973 .

[51]  A. Meyer,et al.  Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. R. Stauffer,et al.  Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. , 1993, Molecular phylogenetics and evolution.

[53]  D. Noakes,et al.  Genetic basis of life history variations among sympatric morphs of arctic char, Salvelinus alpinus. , 1996 .

[54]  R. Vrijenhoek,et al.  Evolution of Fish Species Flocks , 1984 .

[55]  M. Rosenfeld,et al.  Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis , 1999, Nature.

[56]  D. Schluter,et al.  Character displacement and replicate adaptive radiation. , 1993, Trends in ecology & evolution.

[57]  F. Rohlf,et al.  A revolution morphometrics. , 1993, Trends in ecology & evolution.

[58]  D. Kendall MORPHOMETRIC TOOLS FOR LANDMARK DATA: GEOMETRY AND BIOLOGY , 1994 .

[59]  J. Gower Generalized procrustes analysis , 1975 .

[60]  Bernd Fritzsch,et al.  Interspecific fertile hybrids of haplochromine Cichlidae (Teleostei) and their possible importance f , 1983 .

[61]  K. Liem A Functional Approach to the Development of the Head of Teleosts: Implications on Constructional Morphology and Constraints , 1991 .

[62]  B. Grant,et al.  Genetics and the origin of bird species. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[63]  D. Schluter,et al.  The genetic architecture of divergence between threespine stickleback species , 2001, Nature.