Nodal expression and heterochrony in the evolution of dorsal-ventral and left-right axes formation in the direct-developing sea urchin Heliocidaris erythrogramma.
To understand the role of body axes in the evolution of larval form, we use the two sea urchins in the genus Heliocidaris, which have distinctly different larval morphologies. Heliocidaris tuberculata is an indirect-developing sea urchin, which forms a pluteus larva, whereas its sister species, Heliocidaris erythrogramma, exhibits direct development and forms a nonfeeding, ovoid larva. Changes along all three larval axes underlie the differences in larval form associated with each developmental mode. Nodal signaling has recently been implicated as important in establishing the dorsal-ventral (D-V) and left-right (L-R) axes in the indirect-developing sea urchin Paracentrotus lividus. However, because of changes in morphology and timing of morphogenetic events associated with the D-V and L-R axes, respectively, in H. erythrogramma, it was unclear whether nodal played the same roles during direct development. We show that the expression patterns and functions of nodal during H. erythrogramma development are similar to its roles in indirect-developing sea urchins in both D-V and L-R axes formation. However, there are profound changes in gene expression downstream of nodal signaling along the D-V axis and major heterochronies in the execution of the function of nodal along the L-R axis. These highly modified events are linked to the dramatic modifications of larval morphology that have occurred during the evolution of direct development in H. erythrogramma.
Smith
Margaret S
MS
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
Turner
F Rudolf
FR
Raff
Rudolf A
RA
D000818:Animals; D047329:Anthocidaris / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism*; D005075:Biological Evolution; D018507:Gene Expression Regulation, Developmental; D051956:Goosecoid Protein / Q000378:metabolism; D017403:In Situ Hybridization; D007814:Larva / Q000033:anatomy & histology / Q000254:growth & development; D055457:Nodal Protein / Q000235:genetics* / Q000378:metabolism*; D010641:Phenotype; D020133:Reverse Transcriptase Polymerase Chain Reaction; D015398:Signal Transduction; D013997:Time Factors
D051956:Goosecoid Protein; D055457:Nodal Protein