Integration and evolution of the cichlid mandible:The molecular basis of alternate feeding strategiesR. Craig Albertson*†, J. Todd Streelman‡, Thomas D. Kocher§, and Pamela C. Yelick**Department of Cytokine Biology, The Forsyth Institute, and Department of Oral and Developmental Biology, Harvard School of Dental Medicine,Boston, MA 02115;‡School of Biology, Georgia Institute of Technology, Atlanta, GA 30332-0230; and§Hubbard Center for Genome Studies,University of New Hampshire, Durham, NH 03824Edited by David B. Wake, University of California, Berkeley, CA, and approved September 21, 2005 (received for review August 3, 2005)African cichlid fishes have repeatedly evolved highly specializedmodes of feeding through adaptations of their oral jaws. Here, weexplore the molecular genetic basis of the opening and closinglever mechanisms of the cichlid lower jaw, which have traditionallybeen used to describe the mechanics of feeding behavior in bonyfishes. Quantitative genetic analyses demonstrate that the open-ing and closing mechanisms are genetically modular and thereforefree to evolve independently. Bmp4 (bone morphogenetic protein4) is one of two loci that segregate with the mechanical advantageof closing and that together account for >30% of the phenotypicvariance in this trait. Species-specific differences in jaw shape areobvious early in cichlid larval development and are correlated withpatterns of bmp4 expression in the mandibular primordium. Whenbmp4 is overexpressed in the obligate suction feeder Danio rerio,mandibular morphology exhibits specific transformations of open-ing and closing lever ratios. We conclude that patterns of morpho-logical integration of the cichlid jaw reflect a balance amongconflicting functional demands. Further, we demonstrate thatbmp4 has the potential to alter mandibular morphology in a waythat mimics adaptive variation among fish species.adaptive radiation 兩 bmp4 兩 jaw shape 兩 morphological integrationAfundament al divergence among bony fishes occurs betweenspecies that exploit hard and兾or attached prey items andspecies that feed on highly mobile prey. This divergence isc oncomitant with the evolution of stereotypical mandibularmorphologies that reflect the mechanical properties of thefeeding apparatus. Species that prey on hard food evolve short,stout jaws efficient for biting, whereas those that feed on mobileprey of ten evolve elongate, g racile jaws for suction feeding. Thisfunctional dichotomy is exemplified by many perc oid groups,where it is strongly correlated with habitat and morphology. Forexample, shifts along this functional axis are associated with theevolution of North American sunfishes (1, 2). Several coral reeffish lineages exhibit extensive ecological diversity, often associ-ated with elaborate accentuations of biting and suction feeding(3–5). Cichlids have diverged rapidly along this functional axiswith the repeated evolution of alternate biting兾sucking mor-phologies that are characteristic of both deep cladogenic eventsand contemporary fine-scale ecological niche partitioning (6–12). Understanding the molecular basis of changes that differ-entiate biters from suction feeders will lend significant insightinto the adaptive evolution of fish species.The mechanical implications of jaw shape have been wellstudied in fishes (4, 5, 11, 13–16). The teleost mandible can bedescribed as two opposing lever mechanisms: one that definesthe mechanical advantage of closing and another that defines themechan ical advantage of opening. The closing in-lever is mea-sured as the dist ance between the jaw joint and the attachmentof the adductor mandibulae muscle on the coronoid process (Fig.1a, purple line). The opening in-lever is the distance between thejaw joint and the attachment of the interopercular mandibularligament on the retroarticular process (Fig. 1a, green line). Theout-lever is traditionally taken as the dist ance between the jawjoint and the tip of the anteriormost tooth (this measure has beenmodified in our study; see Materials and Methods for justificationand Fig. 1a, blue line). The in-lever-to-out-lever ratio is thef raction of force that is transferred f rom the muscular attach-ment to the distal-most point of the jaw and is referred to as themechan ical advantage (4, 16). Greater mechanical advantageequals greater force transmission, which is optimal for biting,whereas smaller mechanical advantage translates to greatervelocit y transfer, which is t ypical of suction feeders. There is adirect tradeoff bet ween force and velocity, such that species withgreater force transmission will have lower velocity transfer andvice versa (16, 17).The theory of morphological integration postulates that traitsthat function together will also be inherited together, whereasunrelated traits will be inherited independently (18, 19). Implicitto this theory is the concept of modularity. A module is ac omplex of traits integrated by pleiotropy and independent ofother complexes (20). Thus, morphological integration predictsthat functional un its will also be genetically modular. Develop-ment al architecture figures prominently in discussions of mor-phological integration because genetic and functional modular-it y are mediated by developmental processes (21–25).Previous studies have demonstrated that aspects of the cichlidfeeding apparatus are genetically correlated and have evolved inresponse to strong directional selection (26, 27). Here, we testthe specific hypothesis that the cichlid lower jaw is a morpho-logically integrated structure by tracking the segregation offunctional morpholog y in an F2mapping population derivedf rom two cichlid species that employ different modes of feeding.We also explore the potential role of bmp4 (bone morphogeneticprotein 4), a candidate gene for the evolution of craniofacialdiversit y, in regulating lever ratios in the teleost jaw. We showthat patterns of integration and modularity are c onsistent withthe theory of morphological integ ration but that they alsoundersc ore the notion that modularity is a matter of degrees(24); we also show that the underlying genetic architecture of thecichlid jaw reflects the functional and developmental complexityof the anatomy it encodes. In addition, we demonstrate thatbmp4 is associated with and has the potential to alter adaptiveshape differences of the teleost mandible.Materials and MethodsSpecies Rearing and Morphology. We compared two Lake
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