Allocation of cytoplasm to macromeres in embryos of annelids and molluscs is positively correlated with egg size

Abstract

Evolutionary transitions between feeding and nonfeeding larval development have occurred many times in marine invertebrates, but the developmental changes underlying these frequent and ecologically important transitions are poorly known, especially in spiralians. We use phylogenetic comparative methods to test the hypothesis that evolutionary changes in egg size and larval nutritional mode are associated with parallel changes in allocation of cytoplasm to macromere cell lineages in diverse annelids and molluscs. Our analyses show that embryos of species with large eggs and nonfeeding larvae tend to allocate relatively more embryonic cytoplasm to macromeres at 3rd cleavage than do embryos of species with small eggs and feeding larvae. The association between egg size and allocation to macromeres in these spiralians may be driven by constraints associated with mitotic spindle positioning and size, or may be a result of "adaptation in cleavage" to maintain rapid cell cycles in micromeres, position yolk in cell lineages where it can be most efficiently used, or adjust allocation to ectoderm to accommodate changes in embryonic surface area/volume ratio.

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

“…In the majority of annelids and spiralians, the 1Q macromeres acquire a larger size and a larger allocation of cytoplasm and yolk, because the entire trunk ectoderm, mesoderm and endoderm will form from these lineages (Henry, 2014). However, in annelids with small eggs like Owenia , egg size has been correlated with the allocation of cytoplasm to the micromeres and with larval feeding mode (Jones et al, 2016). This reverse ratio between micromere and macromeres is present in another group of annelids, the sipunculans (Boyle and Rice, 2014; Gerould, 1906), where the larger micromere size is thought to contribute to the enlarged amount of apical/anterior ectoderm in the trochophore-like larva of this group, which has big prototrochal cells (Boyle and Rice, 2014).…”

The gastropod foregut — evolution viewed through a developmental lens

“…Studies by Pernet and colleagues (Pernet and McHugh 2010;Pernet et al 2012;Jones et al 2016) have shown that cytoplasm is preferentially sequestered to macromeres during cleavage of annelid and gastropod embryos. A greater amount of cytoplasmic yolk in macromeres (which is typical of lecithotrophic larvae) is correlated with a slowdown in rate of development of midgut structures arising from these macromeres.…”