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Abstract
BackgroundPeriodic patterning of iterative structures is a fundamental process during embryonic organization and development. Studies have shown how gene networks are employed to pattern butterfly eyespots, fly bristles and vertebrate epithelial appendages such as teeth, feathers, hair and mammary glands. Despite knowledge of how these features are organized, little is known about how diversity in periodic patterning is generated in nature. We address this problem through the molecular analysis of oral jaw dental diversity in Lake Malawi cichlids, where closely related species exhibit from 1 to 20 rows of teeth, with total teeth counts ranging from around 10 to 700.ResultsWe investigate the expression of conserved gene networks (involving bmp2, bmp4, eda, edar, fgf8, pax9, pitx2, runx2, shh and wnt7b) known to pattern iterative structures and teeth in other vertebrates. We show that spatiotemporal variation in expression pattern reflects adult morphological diversity among three closely related Malawi cichlid species. Combinatorial epithelial expression of pitx2 and shh appears to govern the competence both of initial tooth sites and future tooth rows. Epithelial wnt7b and mesenchymal eda are expressed in the inter-germ and inter-row regions, and likely regulate the spacing of these shh-positive units. Finally, we used chemical knockdown to demonstrate the fundamental role of hedgehog signalling and initial placode formation in the organization of the periodically patterned cichlid dental programme.ConclusionCoordinated patterns of gene expression differ among Malawi species and prefigure the future-ordered distribution of functional teeth of specific size and spacing. This variation in gene expression among species occurs early in the developmental programme for dental patterning. These data show how a complex multi-rowed vertebrate dentition is organized and how developmental tinkering of conserved gene networks during iterative pattern formation can impact upon the evolution of trophic novelty.
Highlights
Periodic patterning of iterative structures is a fundamental process during embryonic organization and development
We focus on three closely related Lake Malawi cichlids with alternative dental phenotypes (Figure 1): Cynotilapia afra (CA, Figure 1a), a unicuspid species with two tooth rows of large, widely spaced teeth; Metriaclima zebra (MZ, Figure 1b), a bicuspid and tricuspid species with five or six tooth rows of intermediately sized and spaced teeth; and Labeotropheus fuelleborni (LF, Figure 1c), a uniformly tricuspid species with 10 or more tooth rows of small, tightly packed teeth [26,36]
NFiagtuure's1experiment in dental diversity among Lake Malawi cichlids Nature's experiment in dental diversity among Lake Malawi cichlids. (a) Cynotilapia afra (CA) has a crescent-shaped jaw with two rows of widely spaced unicuspid teeth. (b) Metriaclima zebra (MZ) exhibits an intermediate jaw shape with five to six rows of teeth; a first row of bicuspid teeth is followed by several lingual rows of tricuspids. (c) Labeotropheus fuelleborni (LF) has a square-shaped jaw, lined with 10 or more rows of tightly packed tricuspid teeth
Summary
Periodic patterning of iterative structures is a fundamental process during embryonic organization and development. A functionally equivalent field is established along the axis of the oral jaws in most vertebrates, competent to form tooth bud primordia [11,12,13,14,15]. In teleost fish this initial field is known as the primary odontogenic band (OB) [12,13,15] and in mammals it is termed the dental lamina [4,14]. This band or lamina sets the regionally restricted 'field' along the jaw axis from which tooth induction is triggered
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