Key Points
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The segmentation cascade of Drosophila melanogaster is not typical of arthropod segmentation in general, although many of its features are present in other arthropod groups to some extent.
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The earliest stage of the cascade — the maternal-effect genes — has diverged significantly; for example, bicoid function is specific to higher Diptera.
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In insects other than D. melanogaster gap-gene homologues function in determining segmental identity, but the details and specific roles of each gene have diverged. It is possible that the ancestral role of gap genes was to regulate Hox genes, and that these genes were later recruited to regulate segmentation genes.
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At least one pair-rule gene homologue is expressed in a pattern that is consistent with its involvement in segmentation in every arthropod species that has been studied. However, pair-rule periodicity has only been found in a few cases, and could have evolved independently in different lineages.
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The segment polarity gene network is the most conserved aspect of the segmentation cascade. engrailed is involved in defining segmental boundaries in every arthropod species that has been studied.
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There is evidence that the Notch signalling pathway is involved in arthropod segmentation, through a segmentation oscillator that bears many similarities to the vertebrate somitogenesis clock. The oscillator could be an ancestral feature that has been lost in the lineage leading to higher insects.
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The advent of RNAi and transgenesis in non-model arthropods provides the opportunity for functional studies that could extend the understanding of arthropod segmentation beyond the D. melanogaster model.
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Although a model is emerging for how arthropod segmentation evolved, many unanswered questions remain; more data on a wider range of arthropods is needed before the model will be complete.
Abstract
Most of our knowledge about the mechanisms of segmentation in arthropods comes from work on Drosophila melanogaster. In recent years it has become clear that this mechanism is far from universal, and different arthropod groups have distinct modes of segmentation that operate through divergent genetic mechanisms. We review recent data from a range of arthropods, identifying which features of the D. melanogaster segmentation cascade are present in the different groups, and discuss the evolutionary implications of their conserved and divergent aspects. A model is emerging, although slowly, for the way that arthropod segmentation mechanisms have evolved.
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Glossary
- MACROEVOLUTION
-
Evolutionary processes that lead to significant morphological change. This usually refers to processes that occur above the species level.
- LIFE HISTORY
-
The sum of the morphological stages and the ecological environments that an organism goes through during its life.
- BILATERIANS
-
Members of the animal kingdom that have bilateral symmetry — the property of having two similar sides, with definite upper and lower surfaces, and anterior and posterior ends.
- DEUTEROSTOMES
-
One of the three main branches of the bilaterian animals. The deuterostomes include chordates, hemichordates and echinoderms.
- LOPHOTROCHOZOANS
-
One of the three main branches of the bilaterian animals. Lophotrochozoans include annelids, molluscs, flatworms and several other smaller phyla.
- ECDYSOZOANS
-
One of the three main branches of the bilaterian animals. Ecdysozoans are characterized by an unciliated integument, and grow by ecdysis, or moulting. They include nematodes, arthropods and many other smaller phyla.
- SOMITOGENESIS
-
The process of progressive formation, during embryogenesis, of metameric mesodermal units (somites) that represent the precursor structures of dermis, skeletal muscles and the axial skeleton.
- BLASTODERM
-
The layer of cells that completely surrounds an internal mass of yolk in an arthropod embryo.
- FOLLICLE CELLS
-
The somatic cells in Drosophila melanogaster that surround the oocyte; they provide patterning signals to the oocyte and secrete the egg-shell.
- DERIVED
-
Having undergone significant evolutionary change relative to the ancestral state.
- GERM BAND
-
In an arthropod embryo, this is the differentiated portion, which has a distinct anterior–posterior axis, and is where the segmentation process takes place.
- SEGMENT POLARITY GENES
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A group of genes that define different parts of each segmental repeat. When segment polarity genes are mutated the normal number of segments is formed, but these show internal pattern replication and polarity reversals.
- PARASEGMENT
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The initial segmental unit that is formed during the segmentation process. The final segment boundaries lie in the middle of the parasegments.
- HOLOMETABOLOUS
-
Insects for which the life cycle includes distinct larvae, pupae and (usually) winged adults.
- SYNCYTIUM
-
A population of nuclei that are not separated by cell membranes. It is typical of the developing blastoderm in Drosophila melanogaster.
- SHORT GERM
-
A mode of insect development in which anterior segments are patterned in the blastoderm, with posterior segments forming sequentially from a cellularized growth zone after gastrulation.
- HEMIMETABOLOUS
-
Insects for which the life cycle includes several larval stages, ending in a sexually mature, winged adult, without going through a pupal stage.
- MALACOSTRACANS
-
A subclass of crustaceans that includes shrimps, lobsters and sandhoppers.
- AMPHIPODS
-
An order of malacostracan crustaceans that includes beachhoppers.
- PRE-GNATHAL SEGMENTS
-
The gnathal segments comprise the mandibular, maxillary and labial head segments of insects. The pre-gnathal segments lie anterior to these segments. The number of pre-gnathal segments has been debated, but probably includes at least three: the ocular, antennal and intercalary segments.
- BLASTODISC
-
An undifferentiated single-cell layer in an arthropod embryo that ultimately gives rise to all embryonic structures.
- HOX GENES
-
A family of homeodomain transcription factors that are conserved across bilaterian animals; they are expressed in sequence along the A–P axis and are involved in conferring axial identity.
- PROSOMA
-
The anterior part of the body in chelicerates, including the head, the mouthparts and the walking legs.
- OPISTHOSOMA
-
The posterior part of the body in chelicerates. It does not include any walking legs.
- GEOPHILOMORPHS
-
A group of centipedes, normally soil dwelling, that are characterized by a long, thin body made up of many segments (27–191).
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Peel, A., Chipman, A. & Akam, M. Arthropod Segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6, 905–916 (2005). https://doi.org/10.1038/nrg1724
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DOI: https://doi.org/10.1038/nrg1724
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