Short, Long, and Beyond: Molecular and Embryological Approaches to Insect Segmentation

Abstract

Over the past dozen years, studies comparing the expression of orthologues of the Drosophila segmentation genes among various insects have served to broaden our view of the ways in which insects make segments. The molecular data suggest that, although the overall genetic mechanisms of segmentation during embryogenesis have been conserved, the details of this process vary both within and between various insect orders. Here we summarize comparative gene expression data relevant to segmentation with an emphasis on understanding the extent of molecular patterning prior to gastrulation. These results are discussed in embryological context with an eye toward understanding the evolution of segmentation within insects.

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

“…It has been thought that expression of segmentation genes might provide useful shorthand for determining which segments are patterned at the blastoderm. Tribolium blastoderm embryos, for instance, have two stripes of pair-rule gene expression, so it has been inferred that the gnathal and first thoracic segment are patterned in the blastoderm 30 . However, our data point to an apparent ambiguity when comparing segmental fates of marked blastoderm cells with pair-rule stripes.…”

“…As the name implies, elongation in the growth zone has been traditionally assumed to be due to high rates of cell division in the posterior [25][26][27][28] . However, other cellular behaviours-cell migration, cell rearrangements, cell shape change-could be used singly or in combination [29][30][31][32][33][34] . Actual mechanisms of elongation remain poorly described for most arthropods (with the exception of malacostracan crustaceans, which elongate using posterior stem cells 35,36 and the centipede Strigamia maritima, which recruits existing tissue to the elongating germ band 37 ).…”

Ancestral role of caudal genes in axis elongation and segmentation

“…This function of caudal is characteristic of long-germ development, found in Drosophila, where all of the body segments are molecularly determined during the blastoderm stage. This mode is thought to be evolutionarily derived within the higher insects and does not represent the ancestral mode of development (12). On the contrary, short-germ development is found in diverse and phylogenetically basal groups of insects and other arthropods, suggesting that this represents the ancestral mode for generating segments within the arthropods.…”

Extremely small genomes in two unrelated dipteran insects with shared early developmental traits

“…Another developmental factor, egg size, might influence the genome size of dipteran insects as well. Dipterans establish a molecular prepattern of the segmented body in the blastoderm, the monolayer of cells surrounding the yolk before the onset of gastrulation (long-germ development, Davis and Patel 2002). Pattern formation up to this stage proceeds through a cascade of spatially regulated transcription factors in which pair-rule genes, the first genes to become activated in a reiterated pattern of transverse stripes, allocate cells of the blastoderm to alternate segments (Pankratz and Jäckle 1993).…”