Novel Embryogenesis in a Nudibranch Gastropod: Segregation, Expulsion, and Abandonment of Deeply Pigmented Egg Cytoplasm

Abstract

Cases where early development has changed substantially and rapidly, without altering later morphogenesis, can be informative about developmental organization and adaptation. I describe a surprising novelty of early embryogenesis in the arminacean nudibranch Madrella sanguinea from the southeastern coast of Australia. Fertilized eggs of this species segregated a large mass of red-pigmented cytoplasm to the vegetal pole, where much of it was extruded as a type of polar lobe during the first two cleavages. A packet of red material detached from the embryo before the gastrula stage, and these “red bodies” were abandoned when larvae hatched. Segregation of highly pigmented ooplasm and formation of a polar lobe are both unusual among opisthobranch gastropods. Discarding a portion of egg cytoplasm is extremely unorthodox among all animals. Nevertheless, hatched larvae of M. sanguinea underwent typical development for a planktotrophic nudibranch larva, and metamorphosis to a feeding juvenile was induced by the bryozoan prey of the benthic stage. The hypothesis that the red bodies contain a defensive allomone that is provisioned to eggs by the parent requires future testing. The vital role of egg cytoplasm during early development is well illustrated by the many cases in which maternally derived morphogenetic determinants are essential for embryonic patterning. The determinants become differentially segregated within the ooplasm so that they are distributed into different blastomeres during embryonic cleavages (1– 3). These determinants subsequently specify the phenotype of individual blastomeres, without input from neighboring cells. Current understanding of ooplasmic segregation and cell-autonomous specification of embryonic cell fate was greatly facilitated by early embryological studies on ascidians, where qualitative differences in regions of egg cytoplasm can be visualized as distinctive patterns of ooplasmic pigment that change after fertilization (3). Among the spirally cleaving eggs of molluscs, embryonic patterning often results from a combination of regionally segregated morphogenetic determinants and inductive interactions between cells. For example, patellogastropods (true limpets) and euthyneuran gastropods (pulmonates and opisthobranchs) with equally cleaving eggs depend on regional segregation of morphogenetic determinants to specify the animal-vegetal axis (4), but an inductive interaction between micromeres and one of the macromeres later specifies the dorsoventral axis of the embryo (5, 6). Among caenogastropods, ooplasmic segregation of morphogenetic determinants is important for specifying both these axial coordinates. Egg cytoplasm that will be uniquely distributed to the dorsal quadrant of caenogastropod embryos is transiently extruded as a polar lobe during early cleavages (1, 5, 6). A polar lobe has never been reported for eggs of patellogastropods, vetigastropods, or euthyneurans (6). In addition to morphogenetic determinants for embryonic patterning, parents also package nutrients into eggs to provide energy for embryogenesis. Furthermore, recent research has revealed yet another category of maternally derived egg inclusions that has likely resulted from challenges to survival in a hostile external environment. This category includes sunscreens (7), photosynthetic symbionts (8), and secondary metabolites to protect from pathogens or predators (9). Opisthobranch gastropods, particularly nudibranchs, contain many novel secondary metabolites that have a demonstrated or suspected role as feeding deterrents (10–12). At least one species of nudibranch incorporates a defensive Received 10 May 2007; accepted 30 July 2007. E-mail: lpage@uvic.ca Reference: Biol. Bull. 213: 303–306. (December 2007) © 2007 Marine Biological Laboratory