Shared rules of development predict patterns of evolution in vertebrate segmentation

Young, Nathan M.; Winslow, Benjamin; Takkellapati, Sowmya; Kavanagh, Kathryn D.

doi:10.1038/ncomms7690

Cited by 29 publications

(27 citation statements)

References 37 publications

(42 reference statements)

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“…Regardless of the exact molecular details of the interactions between the tooth and the jaw, our analyses suggest organs may outsource specific aspects of morphology to be regulated by adjacent body parts or organs. This kind of physical outsourcing differs from developmental integration in which, for example, adjacent organs affect the size of each other (9,(39)(40)(41). It remains to be explored what kind of organs are more purely selfregulated (genetically and physically), and what kind of organs are more likely to have evolved regulatory feedback mechanisms with surrounding tissues that physically modify shape.…”

Section: Discussionmentioning

confidence: 99%

Mechanical constraint from growing jaw facilitates mammalian dental diversity

Renvoisé

Kavanagh

Lazzari

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Much of the basic information about individual organ development comes from studies using model species. Whereas conservation of gene regulatory networks across higher taxa supports generalizations made from a limited number of species, generality of mechanistic inferences remains to be tested in tissue culture systems. Here, using mammalian tooth explants cultured in isolation, we investigate self-regulation of patterning by comparing developing molars of the mouse, the model species of mammalian research, and the bank vole. A distinct patterning difference between the vole and the mouse molars is the alternate cusp offset present in the vole. Analyses of both species using 3D reconstructions of developing molars and jaws, computational modeling of cusp patterning, and tooth explants cultured with small braces show that correct cusp offset requires constraints on the lateral expansion of the developing tooth. Vole molars cultured without the braces lose their cusp offset, and mouse molars cultured with the braces develop a cusp offset. Our results suggest that cusp offset, which changes frequently in mammalian evolution, is more dependent on the 3D support of the developing jaw than other aspects of tooth shape. This jaw-tooth integration of a specific aspect of the tooth phenotype indicates that organs may outsource specific aspects of their morphology to be regulated by adjacent body parts or organs. Comparative studies of morphologically different species are needed to infer the principles of organogenesis.T he conservation of gene regulatory networks in the development of homologous organs is well exemplified by dentitions. Teeth in fish, reptiles, and mammals have been found to use largely shared developmental gene networks (1, 2). Furthermore, tooth development, similar to organ development in general, results from sequential events that appear to be relatively independent from the development of other organs. In particular, mammalian teeth have been considered highly selfregulatory, as they form inside the dental follicle buffered from the surrounding environment (3-5). The self-regulatory aspect of teeth is further supported by the reiterative use of the same signaling pathways and signaling centers, called enamel knots, present within each growing tooth (2). Experiments on growing teeth have revealed how an activator-inhibitor balance of signaling molecules within a developing tooth and between adjacent teeth regulate dental patterning (6-12).Despite the evidence from mice indicating self-regulation of teeth, several observations suggest an intriguing link between jaw bone and tooth crown formation (3,13,14). In humans, abnormal crown patterns in patients with congenital syphilis have been ascribed to result from infection of the tooth follicle (3). Likewise, loss of function of parathyroid hormone-related protein (PTHrP) leads to loss of alveolar bone resorption and deformation of the tooth crown in the mouse (15)(16)(17)(18)(19). A lethal human syndrome called Blomstrand chondrodysplasia, which invol...

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Section: Discussionmentioning

confidence: 99%

Mechanical constraint from growing jaw facilitates mammalian dental diversity

Renvoisé

Kavanagh

Lazzari

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The concept was soon applied to other tripartite skeletal phenotypes (13). However, the extent of the predictive power of the IC for taxa with less similar (14) and more heterodont (15)(16)(17)(18) dentitions suggests that either the IC mechanism does not characterize these other organisms' dental patterning as specifically or the characterization of the mechanistic output (the phenotype) is not accurately assessed.…”

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confidence: 99%

The integration of quantitative genetics, paleontology, and neontology reveals genetic underpinnings of primate dental evolution

Hlusko

Schmitt

Monson

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

107

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Developmental genetics research on mice provides a relatively sound understanding of the genes necessary and sufficient to make mammalian teeth. However, mouse dentitions are highly derived compared with human dentitions, complicating the application of these insights to human biology. We used quantitative genetic analyses of data from living nonhuman primates and extensive osteological and paleontological collections to refine our assessment of dental phenotypes so that they better represent how the underlying genetic mechanisms actually influence anatomical variation. We identify ratios that better characterize the output of two dental genetic patterning mechanisms for primate dentitions. These two newly defined phenotypes are heritable with no measurable pleiotropic effects. When we consider how these two phenotypes vary across neontological and paleontological datasets, we find that the major Middle Miocene taxonomic shift in primate diversity is characterized by a shift in these two genetic outputs. Our results build on the mouse model by combining quantitative genetics and paleontology, and thereby elucidate how genetic mechanisms likely underlie major events in primate evolution.paleontology | quantitative genetics | primates | neontology | dental variation T he relationship between genotype and phenotype is critical to evolutionary biology, because it influences how phenotypes respond to selective pressures and evolve (1, 2). Paleontologists have long sought to incorporate the etiology of the dental phenotype to inform on questions of environmental, dietary, and adaptive change over time (3)(4)(5)(6). This research has been advanced significantly by the revolution in developmental genetics over the past few decades (7). Experimental research on mice has yielded tremendous biological insight (8). However, for human phenotypes, ranging from inflammation (9) to placentation (10), the limitations of the mouse model due to the ∼140 million years ago of evolution that have occurred since our last common ancestor ∼70 Ma (11) are starting to be recognized. Here, we demonstrate how to overcome the limitations of the mouse model's application to the primate dentition by integrating research from quantitative genetics, neontology, and paleontology. The insights gained from this transdisciplinary approach have implications for all of these seemingly disparate subdisciplines of biology.

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“…Importantly, in all three cases the production of these secondary gradients initiates in an already formed segment, that is, in cells that have been removed from the embryonic field to be patterned. As such, they help to determine and refine the proximal boundaries of the field, while at the same time contribute to segment size control …”

Section: Discussionmentioning

confidence: 99%

“…As such, they help to determine and refine the proximal boundaries of the field, while at the same time contribute to segment size control. 5,74,107 Combining growth-driven displacement of molecular gradients, to establish positional information, with a secondary, self-organizing patterning module appears to be a common design principle in the establishment of periodic patterns. 32 In somitogenesis, the location of segment boundary formation famously depends on the combination of a gradient-dependent, moving "determination front" and cell-intrinsic molecular oscillators.…”

Section: Discussionmentioning

confidence: 99%

“…1,2 The concept of modularity is thus central to our understanding of how repetitive patterns can arise on both developmental and evolutionary timescales. [3][4][5] How then, however, is a certain patterning module repeatedly specified during embryogenesis, in a reliable and robust manner, while at the same time allowing for slight deviations that eventually can be canalized into evolutionarily novel morphologies?…”

Section: Introductionmentioning

confidence: 99%

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A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

Grall

Tschopp

2019

Developmental Dynamics

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Fifty years ago, Lewis Wolpert introduced the concept of “positional information” to explain how patterns form in a multicellular embryonic field. Using morphogen gradients, whose continuous distributions of positional values are discretized via thresholds into distinct cellular states, he provided, at the theoretical level, an elegant solution to the “French Flag problem.” In the intervening years, many experimental studies have lent support to Wolpert's ideas. However, the embryonic patterning of highly repetitive morphological structures, as often occurring in nature, can reveal limitations in the strict implementation of his initial theory, given the number of distinct threshold values that would have to be specified. Here, we review how positional information is complemented to circumvent these inadequacies, to accommodate tissue growth and pattern periodicity. In particular, we focus on functional anatomical assemblies composed of such structures, like the vertebrate spine or tetrapod digits, where the resulting segmented architecture is intrinsically linked to periodic pattern formation and unidirectional growth. These systems integrate positional information and growth with additional patterning cues that, we suggest, increase robustness and evolvability. We discuss different experimental and theoretical models to study such patterning systems, and how the underlying processes are modulated over evolutionary timescales to enable morphological diversification.

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Shared rules of development predict patterns of evolution in vertebrate segmentation

Cited by 29 publications

References 37 publications

Mechanical constraint from growing jaw facilitates mammalian dental diversity

Mechanical constraint from growing jaw facilitates mammalian dental diversity

The integration of quantitative genetics, paleontology, and neontology reveals genetic underpinnings of primate dental evolution

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

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