The evolution of insect wings and spider spinneretsfrom ancestral gills

Arthropods were among the first metazoans to live on land. The transition from an aquatic to terrestrial environment required a number of changes in their morphology and physiology. Some of these changes represent the evolution of novel structures that led to adaptive radiations of specific arthropod lineages. For example, the evolution of insect wings is recognized as the key innovation behind the evolutionary success of the insects, which account for more than 75% of all known metazoan species. Likewise, the evolution and refinement of silk production from spinnerets was a key innovation that led to the evolutionary success of the spider lineage. The evolutionary origins of the insect wing and the spider spinneret are not clearly delineated in the fossil record, but molecular evidence suggests that these disparate structures may each be derived from the gills of ancestral arthropods.

Insect wings arose once during evolution, and the first wing-like structures, which may have been used for respiration or osmoregulation, appeared on each trunk segment of aquatic insect larvae in the early Carboniferous. Over the early course of insect evolution, wings became restricted to the adult thorax (see Chapter 5). At first, these structures might have allowed insects to skim across water surfaces; later, they evolved the ability to sustain gliding and powered flight. The earliest spider fossils document the presence of spinnerets on the opisthosomal segments, suggesting that silk was already in use during the early stages of spider evolution. Refinements in silk production, combined with changes in the positioning of the spinnerets and structure of the tarsal claws allowed spiders to use woven silk for multiple purposes. Just as flight allowed insects to escape predation, to catch prey, and to move to other habitats, silk provided spiders similar advantages via droplines, webs, and ballooning. The opportunities presented by these unique characters catalyzed the evolutionary radiation of the insect and spider lineages.

One hypothesis concerning the morphological origin of insect wings suggests that the wing evolved from a dorsal branch (epipodite) of a multibranched crustacean limb (Fig. 6.2a). In this scenario, the fusion of the base of the ancestral branched insect limb with the body wall led to the evolutionary displacement of the wing/epipodite away from the rest of the leg. This model also predicts that developmental regulatory similarities between insect wings and crustacean epipodites should reflect their common ancestry.

Indeed, the expression patterns of homologs of two Drosophila wing-patterning genes in crustacean appendages are consistent with the origination of insect wings from a dorsal limb branch in an ancestral arthropod. In the crayfish, the pdm gene is expressed in two distinct domains of the multibranched thoracic limb that are reminiscent of the two patterns of pdm (also known as nubbin) expression in the fly wing and leg, respectively. The pdm gene is expressed throughout a dorsal epipodite in crayfish thoracic limbs, much like the pattern observed in Drosophila wing imaginal discs, and in rings in the ventral, walking branch of crayfish thoracic limbs, much like the pattern seen in developing Drosophila legs (Fig. 6.2b,c).

Insect Molecular Genetics

Insect thoracic appendages

Ancestral multibranched i appendage

Insect thoracic appendages

Ancestral multibranched i appendage

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