The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella

Abstract

Adelphophagy occurs when encapsulated embryos complete development by feeding on their developing siblings, which are known as nutritive embryos. Nutritive embryos are found in a variety of animal groups, and are especially common in some groups of marine invertebrates. Although they have evolved numerous times independently in the calyptraeid gastropods, adelphophagic development with nutritive embryos has not been described in detail. Using light microscopy and time-lapse imaging of laboratory-reared embryos, we describe the development of Crepidula navicella, a direct developer with nutritive embryos that cleave and gastrulate. Early stages of nutritive and viable embryos do not show any obvious morphological differences, but do show asynchrony in early cleavage among embryos from the same capsule. We discovered that two classes of nutritive embryos are produced; gastrula-like nutritive embryos, which arrest after gastrulation, and post-gastrula-like nutritive embryos that are more variable in morphology, and show evidence of minor differentiation. This study provides a framework for future research on the developmental and molecular mechanisms of nutritive embryo development of C. navicella, which will allow us to address the role of nutritive embryos in the origins of developmental polyphenisms. Careful description of the developmental sequence is necessary before adaptive hypotheses can be addressed, and comparisons with other taxa can be made. Understanding the different ways that embryos and their development are disrupted to produce nutritive embryos will provide important insights into the normal process of development.

Early Activation of MAPK and Apoptosis in Nutritive Embryos of Calyptraeid Gastropods

“…Development of C. fornicata has been well characterized (Conklin, , Henry et al., , Hejnol et al., , Lyons et al., , Lyons et al., , Perry et al., ), and all embryos develop into normal veliger larvae. In contrast, more than 90% of embryos produced by C. navicella will become nutritive embryos (Lesoway et al., ). The number of viable embryos produced in C. lichen is more variable, as females can produce either broods of all viable embryos or mixed broods containing nutritive embryos (McDonald et al., ).…”

“…Adult females of C . navicella Lesson 1831, C. lichen Broderip 1834 and Crepidula lessoni Broderip 1834 were collected from Playa Venado near Veracruz, Panama (8°52.9567′N, 79°35.8778′W) and returned to Naos Marine Laboratories at the Smithsonian Tropical Research Institute (STRI) for culture as described previously (Lesoway et al., ). Live adults were also transported to McGill University (Montreal, Canada), where they were kept in a 45‐L aquarium with a hang on back filter, and maintained at approximately 27°C and a salinity of 32 ppt.…”

“…Also known as trophic or nurse embryos, they are found in a variety of animal groups, and are well represented in marine invertebrates, particularly polychaetes and gastropods (Thorson, , Fioroni, , Elgar and Crespi, , Martín‐Durán et al., ). Development of nutritive embryos has been described in detail in the direct developing species Crepidula navicella (Lesoway et al., , ). In C. navicella , all embryos begin to develop normally, however, fewer than 10% will develop into viable embryos; the remainder will become nutritive embryos.…”

“…Shortly after gastrulation, viable embryos show visible signs of differentiation and nutritive embryo identity can be confirmed. Nutritive embryos in C. navicella can be further categorized into gastrula‐like nutritive embryos that arrest development at the gastrula stage, and postgastrula‐like nutritive embryos that arrest development at a slightly later stage of development and show limited differentiation (Lesoway et al., ).…”

Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia

“…As marine animals develop, they are confronted with the task of maintaining a balance between energy intake and energy consumption (Chaparro and Paschke, 1990;Bayne, 2004). Those embryos and larvae that undergo encapsulated development are dependent on maternal provisioning for their energy supply, which can occur extra-embryonically through additional nurse eggs (Rivest, 1983;Chaparro and Paschke, 1990), cannibalism (adelophagy) (Lesoway et al, 2014;Thomsen et al, 2014) or albumen deposited within the egg capsule by the mother at the time of laying (Moran, 1999). The development rate of marine embryos and larvae has been linked to the maternal provisioning they receive.…”