Heads and tails: evolution of antero-posterior patterning in insects

Abstract

In spite of their varied appearances, insects share a common body plan whose layout is established by patterning genes during embryogenesis. We understand in great molecular detail how the Drosophila embryo patterns its segments. However, Drosophila has a type of embryogenesis that is highly derived and varies extensively as compared to most insects. Therefore, the study of other insects is invaluable for piecing together how the ancestor of all insects established its segmented body plan, and how this process can be plastic during evolution. In this review, we discuss the evolution of Antero-Posterior (A-P) patterning mechanisms in insects. We first describe two distinct modes of insect development - long and short germ development - and how these two modes of patterning are achieved. We then summarize how A-P patterning occurs in the long-germ Drosophila, where most of our knowledge comes from, and in the well-studied short-germ insect, Tribolium. Finally, using examples from other insects, we highlight differences in patterns of expression, which suggest foci of evolutionary change.

Figure 1. Schematic representation of long germ and short germ embryos

(A) Lateral view. In long germ embryos, relatively little of the egg is allocated for extraembryonic tissues (blue dots), while the germ occupies the majority. The germ rudiment of short germ insects is restricted to the ventral posterior of the blastoderm, while the remainder of the egg is occupied by extraembryonic tissues. (B) Ventral view. In long germ insects, all of the future segments (head [H], thorax [T] and abdomen [A]) will be patterned in the precellular blastoderm by two patterning centers (indicated by stars). Short germ insects pattern only head and thorax before gastrulation, from a single patterning center at the posterior.

Figure 2. Schematic representation of segmentation gene expression patterns in long and short germ insects

Patterning centers are indicated by stars and non-germ tissue by blue dots. Stripes indicate approximate domains of gene expression, triangles indicate morphogen gradients. Abbreviations: Ac- acron; H-head; Th- thorax; Ab- abdomen; Tel- telson.

Figure 3. Model for transition from short germ to long germ mode of embryogenesis

In the first step, the germ is expanded anteriorly, for instance, through reduction of Zen expression. Second, an anterior patterning center is acquired to localize morphogens near the future head. Lastly, gap gene boundaries, such as Kr, shift anteriorly, leaving room for patterning of abdominal segments from the remaining blastoderm. Patterning centers are indicated by stars, and extraembryonic tissues by blue dots. Abbreviations: H- head; Th-thorax; Ab- abdomen.