Germ cell specification, syncytial development, and egg diversity in insects

Abstract

Evolutionary changes in development have generated a vast diversity of multicellular forms. This dissertation, taken as a whole, is an effort to discern patterns in that evolutionary process. Each individual chapter is a joint effort with one or more collaborators to address open questions in insect development, often using the embryogenesis of the cricket Gryllus bimaculatus as an example case. In Chapter 1, we show that Bone Morphogenic Protein (BMP) signaling is necessary for the specification of germ cells in the cricket G. bimaculatus. Next, we develop two resources for the study of comparative development in insects: Chapter 2 is a description of the morphological development of embryos of G. bimaculatus, as viewed from outside the egg and in dissected embryos. This work includes time-lapse microscopy, an updated developmental staging table, and a review of published gene expression patterns. In Chapter 3, we prototype and test techniques for mounting and live-imaging many embryos at once. Then, in Chapter 4 we use the products of the previous two chapters to delve more deeply into the events that occur immediately after fertilization in G. bimaculatus. For most insect species, the earliest stage of development is a syncytium—many nuclei sharing a single large cytoplasm. The nuclei divide and move, ultimately cellularizing and forming the organized rudiment of the embryo. We study this process in G. bimaculatus using lightsheet microscopy, experimental manipulations, and computational modeling. We develop hypotheses for how the nuclei move throughout the egg and how mechanical forces might restrict cell fates in the early cricket embryo. Finally, in Chapter 5 we assemble a dataset of over 10,000 published records of insect egg size and shape. We use comparative phylogenetic methods to assess whether features of egg evolution are associated with ecological and embryological variables. Then, we reconstruct ancestral states of insect eggs and test several published hypotheses about the patterns of egg evolution.