Two or Four Bristles: Functional Evolution of an Enhancer of scute in Drosophilidae

A central challenge in evolutionary biology is understanding how genetic mutations underlie morphological changes. Because highly calcified enamel enables preservation of detailed dental features, studying tooth morphology enables this question to be addressed in both extinct and extant species. Previous studies have found that mutant mice can have severe abnormalities in tooth morphology, and several authors have explored the evolutionary implications of tooth number modifications in mutants. However, although they can potentially shed much light on evolutionary mechanisms, anomalies in tooth shape remain poorly studied. Here, we report that alterations in dosage of the Fgf3 gene cause morphological changes in both genetically engineered mutant mice and in human patients. By comparing the dental morphologies in mice and humans carrying Fgf3 mutations with primitive rodent and primate fossils, we determined that decreases in dosage of Fgf3 lead to phenotypes that resemble the progressive reappearance of ancestral morphologies. We propose that modifications in the FGF signaling pathway have played an important role in evolution of mammalian dentition by giving rise to new cusps and interconnecting cusps by new crests. We anticipate that our multidisciplinary study will advance the detailed correlation of subtle dental modifications with genetic mutations in a variety of mammalian lineages. dental morphology ͉ Muroidea ͉ primates

Section: Humans Carrying Fgf3 Mutations Have Similar Dental Morphologsupporting

confidence: 49%

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

Charles

Lazzari

Tafforeau

et al. 2009

“…factors involved in regulating these CREs and other case studies of morphological divergence among closely related species or populations (21,22,(31)(32)(33)(34)(35) illustrate what we submit are general insights into the process of evolution by gene regulation.…”

Section: Pigmentation Patterns and Gene Expression As Models Of Regulmentioning

confidence: 67%

Emerging principles of regulatory evolution

Prud’homme

Gompel

Carroll

2007

473

426

Understanding the genetic and molecular mechanisms governing the evolution of morphology is a major challenge in biology. Because most animals share a conserved repertoire of body-building and -patterning genes, morphological diversity appears to evolve primarily through changes in the deployment of these genes during development. The complex expression patterns of developmentally regulated genes are typically controlled by numerous independent cis-regulatory elements (CREs). It has been proposed that morphological evolution relies predominantly on changes in the architecture of gene regulatory networks and in particular on functional changes within CREs. Here, we discuss recent experimental studies that support this hypothesis and reveal some unanticipated features of how regulatory evolution occurs. From this growing body of evidence, we identify three key operating principles underlying regulatory evolution, that is, how regulatory evolution: (i) uses available genetic components in the form of preexisting and active transcription factors and CREs to generate novelty; (ii) minimizes the penalty to overall fitness by introducing discrete changes in gene expression; and (iii) allows interactions to arise among any transcription factor and downstream CRE. These principles endow regulatory evolution with a vast creative potential that accounts for both relatively modest morphological differences among closely related species and more profound anatomical divergences among groups at higher taxonomical levels.pleiotropy ͉ cis-regulation ͉ transcription ͉ pigmentation ͉ body plan

“…Thus, it seems unlikely that the patterning differences between the species are driven by changes in the cis-regulatory architecture of the surveyed genes. The scenario might be different for traits like thorax bristles and wing pigmentation, where recent evidence illustrates the role of cis-regulatory evolution (34)(35)(36).…”

Section: Discussionmentioning

confidence: 99%

Canalization of segmentation and its evolution in Drosophila

Lott

Kreitman

Pálsson

et al. 2007

155

Segmentation in Drosophila embryogenesis occurs through a hierarchical cascade of regulatory gene expression driven by the establishment of a diffusion-mediated morphogen gradient. Here, we investigate the response of this pattern formation process to genetic variation and evolution in egg size. Specifically, we ask whether spatial localization of gap genes Kruppel (Kr) and giant (gt) and the pair-rule gene even-skipped (eve) during cellularization is robust to genetic variation in embryo length in three Drosophila melanogaster isolines and two closely related species. We identified two wild-derived strains of D. melanogaster whose eggs differ by Ϸ25% in length when reared under identical conditions. These two lines, a D. melanogaster laboratory stock (w1118), and offspring from crosses between the lines all exhibit precise scaling in the placement of gap and pair-rule gene expression along the anterior-posterior axis in relation to embryo length. Genetic analysis indicates that this scaling is maternally controlled. Maternal regulation of scaling must be required for consistent localization of segmentation gene expression because embryo size, a genetically variable and adaptive trait, is maternally inherited. We also investigated spatial scaling between these D. melanogaster lines and single lines of Drosophila sechellia and Drosophila simulans, the latter two differing by Ϸ25% in egg length. In contrast to the robust scaling we observed within species, localization of gene expression relative to embryo length differs significantly between the three species. Thus, the developmental mechanism that assures robust scaling within a species does not prevent rapid evolution between species.buffering ͉ development ͉ embryo size ͉ genetic variation ͉ scaling