Society for Developmental Biology meeting summary

Interesting paper

Evolution of development in the sea star genus Patiriella: clade-specific alterations in cleavage

Anna Cerra Maria Byrne

Abstract

Examination of early development in five species of the Patiriella sea star species complex indicates that the ancestral-type radial holoblastic cleavage (Type I) is characteristic of P. regularis and P. exigua, whereas cleavage in species from the calcar clade followed multiple alternatives (Types II–IV) from holoblastic to meroblastic. Considering that invariant radial cleavage is thought to play a role in embryonic axis formation in echinoderms, we documented the details of blastomere formation in Patiriella sp. and followed development of the embryos. In Type II cleavage, the first and second cleavage planes appeared simultaneously at one pole of the embryo, dividing it directly into four equally sized blastomeres. In Type III cleavage, the first and second cleavage planes appeared simultaneously, followed promptly by the third cleavage plane, dividing the embryo directly into eight equally sized blastomeres. In Type IV cleavage, numerous furrows appeared simultaneously at one end of the embryo, dividing it into 32–40 equally sized blastomeres. Confocal sections revealed that embryos with cleavage Types II–IV were initially syncytial. The timing of karyokinesis in embryos with Types II and III cleavage was similar to that seen in clutch mates with Type I cleavage. Karyokinesis in embryos with Type IV cleavage, however, differed in timing compared with Type I clutch mates. Alteration in cleavage was not associated with polarized distribution of maternally provided nutrients. For each cleavage type, development was normal to the competent larval stage. Although variable blastomere configuration in the calcar clade may be linked to possession of a lecithotrophic development, other Patiriella species with this mode of development have typical cleavage. The presence of variable cleavage in all calcar clade species indicates that phylogenetic history has played a role in the distribution of this embryonic trait in Patiriella. The plasticity in early cleavage in these sea stars indicates that this aspect of early development is not constrained against change and that there are many ways to achieve multicellularity.

Nelson Wrote:

Reviewing these fundamental differences, Grbic muses, “It is hard to conceptualize the evolution of a novel stage that disrupts one of the crucial paradigms of Drosophila development, maternal specification of the embryonic axis” (Grbic 2003, p. 640).

From the paper

It is hard to conceptualize how is the proliferative stage integrated with de novo establishment of embryonic axes. All 2000 embryo axes appear to form independently with random axial orientation relative to each other (Grbic et al., 1996b). This favours an independent specification of the axial polarity within each embryo rather than a global mechanism specifying simultaneous polarity in 2000 embryos. However, recent genetic analysis of the basal long germband wasp reveals differences relative to fly development that could be utilized to develop the model of evolution of polyembryony. Genetic analysis of the long germ ectoparasitic wasp Nasonia virtripennis revealed mutations in embryo pattern that correspond to putative gap and pair-rule mutant phenotypes in Drosophila, as well as zygotic phenotypes that have no fly mutant counterparts (Pultz et al., 1999). Most importantly, it appears that in Nasonia zygotic control has a more prominent effect on embryo patterning, contrasting predominantly maternal early control as determined in the fly (Pultz et al., 1999). It is hard to conceive that at the stage of embryonic primordium (and during its formation) a Drosophila-like transcription gradient operates in the cellular environment of Copidosoma and Macrocentrus embryos. However, gap genes appear to be involved in embryo patterning in both wasps. It is possible that the predominance of zygotic control of embryo patterning in the ancestral long germband wasps such as Nasonia could be used as a stepping stone to shift embryo patterning to the zygotic genes at the late stages of embryogenesis (following the proliferation) and thus allow “insertion” of the proliferative stage. However, this still does not explain how de novo axial polarity is initiated at the polyembryonic blastoderm. Emerging evolutionary flexibility of early genes involved in polarization of the embryonic axis in insects suggests that it is impossible to use the candidate gene approach based on the Drosophila paradigm to isolate the earliest axial organizers in polyembryonic wasps. The cellular environment in endoparasitic wasps narrows the choice of genes to a group of signaling genes that are used in other systems to establish embryonic axis. Current knowledge of the patterning of polyembryonic and monoembryonic wasps suggests two approaches to isolate putative genes involved in de novo establishment of axial polarity. One approach would be to utilize genomic EST expression screens in both monoembryonic holoblastic cleaving and polyembryonic wasps to isolate those that are expressed at the future embryo poles. In addition, isolation of the regulatory regions of Kruppel could serve as a tool in determining the gene products binding to its regulatory regions in Copidosoma and Macrocentrus. This could provide clues as to how the conserved phase of the gap patterning cascade is integrated with the regulatory elements directing de novo establishment of axial polarity.