The role of wingless in the development of multibranched crustacean limbs.
Arthropods are the most diverse and speciose group of organisms on earth. A key feature in their successful radiation is the ease with which various appendages become readily adapted to new functions in novel environments. Arthropod limbs differ radically in form and function, from unbranched walking legs to multibranched swimming paddles. To uncover the developmental and genetic mechanisms underlying this diversification in form, we ask whether a three-signal model of limb growth based on Drosophila experiments is used in the development of arthropod limbs with variant shape. We cloned a Wnt-1 ortholog (Tlwnt-1) from Triops longicaudatus, a basal crustacean with a multibranched limb. We examined the mRNA in situ hybridization pattern during larval development to determine whether changes in wg expression are correlated with innovation in limb form. During larval growth and segmentation Tlwnt-1 is expressed in a segmentally reiterated pattern in the trunk. Unexpectedly, this pattern is restricted to the ventral portion of the epidermis. During early limb formation the single continuous stripe of Tlwnt-1 expression in each segment becomes ventrolaterally restricted into a series of shorter stripes. Some but not all of these shorter stripes correspond to what becomes the ventral side of a developing limb branch. We conclude that the Drosophila model of limb development cannot explain all types of arthropod proximodistal outgrowths, and that the multibranched limb of Triops develops from an early reorganization of the ventral body wall. In Triops, Tlwnt-1 plays a semiconservative role similar to that played by Drosophila wingless in segmentation and limb formation, and morphological innovation in limb form arises in part through an early modulation in the expression of the Tlwnt-1 gene.
Nulsen
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Department of Cell Biology and Anatomy, University of Arizona, Tucson, AZ 85721, USA. cnulsen@u.arizona.edu
Nagy
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LM
D000595:Amino Acid Sequence; D000818:Animals; D019521:Body Patterning / Q000235:genetics; D003001:Cloning, Molecular; D033364:Decapoda / Q000737:chemistry / Q000196:embryology / Q000235:genetics*; D029721:Drosophila Proteins; D005121:Extremities / Q000033:anatomy & histology / Q000196:embryology*; D018507:Gene Expression Regulation, Developmental; D006257:Head / Q000033:anatomy & histology / Q000196:embryology; D017403:In Situ Hybridization; D008969:Molecular Sequence Data; D011518:Proto-Oncogene Proteins / Q000235:genetics / Q000502:physiology*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D014018:Tissue Distribution; D051153:Wnt Proteins; D051155:Wnt1 Protein; D029961:Zebrafish Proteins
D029721:Drosophila Proteins; D011518:Proto-Oncogene Proteins; D012333:RNA, Messenger; D051153:Wnt Proteins; D051155:Wnt1 Protein; D029961:Zebrafish Proteins; C074622:wg protein, Drosophila