Correct fate specification depends on cells being in the right place at the right time. In insects, this problem is one of nuclear positioning, since early embryos are syncytial: the first embryonic cleavages consist of rounds of synchronous mitoses without cytokinesis. The early embryo is thus a single cell containing hundreds of nuclei that move from initial positions deep in the yolk into a uniform cortical blastoderm, putting nuclei in place to receive the fate specification information waiting for them in each cytoplasmic region. The mechanisms driving this movement remain largely unknown, and actinomyosin-driven cytoplasmic flows that explain some late blastoderm nuclear movements in Drosophila cannot explain the nuclear movements that create the blastoderm in the first place. We therefore use lightsheet microscopy to image nucleus movements in live transgenic cricket embryos (Gryllus bimaculatus), and apply quantitative image analysis to the data. In collaboration with the Rycroft lab (Harvard Applied Math), we generated mathematical models predicting nuclear behaviour (shown in the movie above), which we subsequently verified experimentally. We discovered that nuclei “sense” both other nuclei near them and their proximity to the eggshell, and use this information to make local decisions about their division, direction and speed of movement. Our work may provide general insight into the mechanisms that ensure correct nuclear positioning within multiple types of syncytial cells. Future work will determine whether and how these movements are constrained by the shape and size of the egg, and whether they play a role in the crucial fate decision that separates embryonic from extra-embryonic cells.
These seed-like eggs are laid by the northern walking stick, Diapheromera femorata. The background is an array of egg shape silhouettes reconstructed from drawings in the entomological literature. Eggs were imaged by Sofia Prado-Irwin, Bruno de Medeiros, and Samuel Church at the The Caterpillar Lab in Keane, NH; and depicted with egg silhouettes by Seth Donoughe.
The gamete is the homologous single-celled stage shared by all animals, and it gives rise to the egg, which is the arena for embryonic development. Our study of the evolution of embryonic development therefore includes consideration of how the egg evolved, how its development and function are regulated, how it impacts embryonic organization and function, and the factors that continue to influence its evolution in natural environments. By applying modern phylogenetic comparative methods to four centuries’ worth of empirical observations on insect egg size and shape, we showed that the evolutionary dynamics of egg morphospace defy long-standing claims of universal scaling laws governing the evolution of allometry. In an illustration of the potential impact of environment on heritable phenotypes, we showed that the ecological context where eggs are laid is the best predictor of egg morphology.
Development from zygote to hatchling occurs through a complex and coordinated series of mitotic divisions, or cleavages. Many arthropods, particularly crustaceans, display a stereotyped pattern of early cleavage. In the amphipod crustacean Parhyale hawaiensis, at least some cell fates are normally established by inheritance of a morphologically distinct cytoplasmic region in the one-cell embryo. Removal of this cytoplasmic region can results in a loss of the embryonic cells that would have normally inherited it. However, in some cases it can also cause changes in the behavior of other early cleavage blastomeres, including changing their cell fates, resulting in regulative regeneration in embryonic and post-embryonic stages. Using many different types of microscopy, we are establishing a complete cell lineage over space and time for the early stages of the P. hawaiensis embryo. This work provides the basis for continued research into the molecular genetic mechanisms underlying cell fate acquisition, cell fate plasticity, and early embryonic cell movements.
Reconstruction of early embryonic divisions and cell movements in Parhyale hawaiensis, derived from analysis of lightsheet data. Spheres indicate nuclear positions in 4D, and colors indicate germ layer lineage. Blue: ectoderm; red, orange & pink: mesoderm; green: endoderm; yellow: germ line.
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