Integration and evolution of the cichlid mandible The molecular basis of alternate feeding strategies R 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 03824 African cichlid fishes have repeatedly evolved highly specialized modes of feeding through adaptations of their oral jaws Here we explore the molecular genetic basis of the opening and closing lever mechanisms of the cichlid lower jaw which have traditionally been used to describe the mechanics of feeding behavior in bony fishes Quantitative genetic analyses demonstrate that the opening and closing mechanisms are genetically modular and therefore free to evolve independently Bmp4 bone morphogenetic protein 4 is one of two loci that segregate with the mechanical advantage of closing and that together account for 30 of the phenotypic variance in this trait Species specific differences in jaw shape are obvious early in cichlid larval development and are correlated with patterns of bmp4 expression in the mandibular primordium When bmp4 is overexpressed in the obligate suction feeder Danio rerio mandibular morphology exhibits specific transformations of opening and closing lever ratios We conclude that patterns of morphological integration of the cichlid jaw reflect a balance among conflicting functional demands Further we demonstrate that bmp4 has the potential to alter mandibular morphology in a way that mimics adaptive variation among fish species adaptive radiation bmp4 jaw shape morphological integration A fundamental divergence among bony fishes occurs between species that exploit hard and or attached prey items and species that feed on highly mobile prey This divergence is concomitant with the evolution of stereotypical mandibular morphologies that reflect the mechanical properties of the feeding apparatus Species that prey on hard food evolve short stout jaws efficient for biting whereas those that feed on mobile prey often evolve elongate gracile jaws for suction feeding This functional dichotomy is exemplified by many percoid groups where it is strongly correlated with habitat and morphology For example shifts along this functional axis are associated with the evolution of North American sunfishes 1 2 Several coral reef fish lineages exhibit extensive ecological diversity often associated with elaborate accentuations of biting and suction feeding 3 5 Cichlids have diverged rapidly along this functional axis with the repeated evolution of alternate biting sucking morphologies that are characteristic of both deep cladogenic events and contemporary fine scale ecological niche partitioning 6 12 Understanding the molecular basis of changes that differentiate biters from suction feeders will lend significant insight into the adaptive evolution of fish species The mechanical implications of jaw shape have been well studied in fishes 4 5 11 13 16 The teleost mandible can be described as two opposing lever mechanisms one that defines the mechanical advantage of closing and another that defines the mechanical advantage of opening The closing in lever is measured as the distance between the jaw joint and the attachment of the adductor mandibulae muscle on the coronoid process Fig 1a purple line The opening in lever is the distance between the jaw joint and the attachment of the interopercular mandibular ligament on the retroarticular process Fig 1a green line The out lever is traditionally taken as the distance between the jaw www pnas org cgi doi 10 1073 pnas 0506649102 joint and the tip of the anteriormost tooth this measure has been modified in our study see Materials and Methods for justification and Fig 1a blue line The in lever to out lever ratio is the fraction of force that is transferred from the muscular attachment to the distal most point of the jaw and is referred to as the mechanical advantage 4 16 Greater mechanical advantage equals greater force transmission which is optimal for biting whereas smaller mechanical advantage translates to greater velocity transfer which is typical of suction feeders There is a direct tradeoff between force and velocity such that species with greater force transmission will have lower velocity transfer and vice versa 16 17 The theory of morphological integration postulates that traits that function together will also be inherited together whereas unrelated traits will be inherited independently 18 19 Implicit to this theory is the concept of modularity A module is a complex of traits integrated by pleiotropy and independent of other complexes 20 Thus morphological integration predicts that functional units will also be genetically modular Developmental architecture figures prominently in discussions of morphological integration because genetic and functional modularity are mediated by developmental processes 21 25 Previous studies have demonstrated that aspects of the cichlid feeding apparatus are genetically correlated and have evolved in response to strong directional selection 26 27 Here we test the specific hypothesis that the cichlid lower jaw is a morphologically integrated structure by tracking the segregation of functional morphology in an F2 mapping population derived from two cichlid species that employ different modes of feeding We also explore the potential role of bmp4 bone morphogenetic protein 4 a candidate gene for the evolution of craniofacial diversity in regulating lever ratios in the teleost jaw We show that patterns of integration and modularity are consistent with the theory of morphological integration but that they also underscore the notion that modularity is a matter of degrees 24 we also show that the underlying genetic architecture of the cichlid jaw reflects the functional and developmental complexity of the anatomy it encodes In addition we demonstrate that bmp4 is associated with and has the potential to alter adaptive shape differences of the teleost mandible Materials and Methods Species Rearing and Morphology We compared two Lake Malawi rock dwelling cichlid species with distinct feeding behaviors and jaw morphologies 28 Labeotropheus fuelleborni LF is a specialized biting species characterized by a short stout lower jaw with high
View Full Document
Unlocking...