Evolution of homeotic gene regulation and function in flies and butterflies

Diversification of leg appendages is one of the hallmarks of morphological evolution in insects. In particular, insect hind (T3) legs exhibit a whole spectrum of morphological diversification, ranging from uniform to extremely modified. To elucidate the developmental basis of T3 leg evolution, we have examined the expression patterns of two homeotic genes, Ultrabithorax and abdominal-A (collectively referred to as UbdA), in a broad range of species. First, our results show that UbdA expression in hemimetabolous insects is localized only in specific T3 leg segments undergoing differential growth (compared to their foreleg counterparts). In contrast, in basal hexapod and insect lineages, the absence of the UbdA signal coincides with uniform leg morphology. The same situation exists in first instar larvae of holometabolous insects, in which absence of UbdA expression in the embryonic T3 legs is associated with the lack of larval T3 leg diversification. Second, there is a clear difference in the timing of expression between species with greatly enlarged T3 leg, such as crickets and grasshoppers, and species that exhibit more moderate enlargement of hind legs, such as mantids and cockroaches. In the former, the UbdA expression starts much earlier, coinciding with the elongation of T3 limb buds. In the latter, however, the UbdA expression starts at much later stages of development, coinciding with the establishment of distinct leg segments. These results suggest that diversification of insect hind legs was influenced by changes in both the spatial and temporal regulation of the UbdA expression.

Section: Ubda Expression In Insects With Moderately Enlarged Hind Legssupporting

confidence: 74%

Section: Ubda Expression In Insects With Moderately Enlarged Hind Legsmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Differential expression patterns of the hox gene are associated with differential growth of insect hind legs

Mahfooz

Popadić

2004

“…In Drosophila, the Hox protein Ubx, which is expressed in the T3 segment and appendages, controls the differentiation between wing and haltere (61,62). Because Ubx is also expressed in the developing hindwings of four-winged insects (63), the evolutionary reduction of the hindwing in Diptera occurred under the control of the Ubx protein and did not result from a shift of the expression of Ubx. In the Drosophila haltere, Ubx directly represses the expression of a set of wing-patterning genes (64,65).…”

Section: Connecting the Dots From Pigmentation Patterns To Body Plan mentioning

confidence: 99%

Emerging principles of regulatory evolution

Prud’homme

Gompel

Carroll

2007

484

440

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

“…For example, changes in Hox gene regulation (2)(3)(4)(5)(6), in Hox coding sequences (7,8), and in the interactions of Hox genes with their downstream targets (9,10) have all been implicated in the evolution of segment diversity in arthropods.…”

mentioning

confidence: 99%

Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean

Pavlopoulos¹,

Kontarakis

Liubicich

et al. 2009

Changes in the expression of Hox genes have been widely linked to the evolution of animal body plans, but functional demonstrations of this relationship have been impeded by the lack of suitable model organisms. A classic case study involves the repeated evolution of specialized feeding appendages, called maxillipeds, from anterior thoracic legs, in many crustacean lineages. These leg-to-maxilliped transformations correlate with the loss of Ultrabithorax (Ubx) expression from corresponding segments, which is proposed to be the underlying genetic cause. To functionally test this hypothesis, we establish tools for conditional misexpression and use these to misexpress Ubx in the crustacean Parhyale hawaiensis. Ectopic Ubx leads to homeotic transformations of anterior appendages toward more posterior thoracic fates, including maxilliped-to-leg transformations, confirming the capacity of Ubx to control thoracic (leg) versus gnathal (feeding) segmental identities. We find that maxillipeds not only are specified in the absence of Ubx, but also can develop in the presence of low/transient Ubx expression. Our findings suggest a path for the gradual evolutionary transition from thoracic legs to maxillipeds, in which stepwise changes in Hox gene expression have brought about this striking morphological and functional transformation.functional studies ͉ maxillipeds ͉ morphological evolution ͉ Parhyale ͉ Ultrabithorax (Ubx)