Flight II: Evolution of Wings and Flight

• What structures gave rise to wings?

• What functions did these structures serve before they were wings?

• Did wings evolve more than once in insects?

• Why are functional wings found only in the adult stage of insects?

• Why aren’t wings in intermediate stages of development found in the fossil record, or in extant insects?

Major questions concerning the evolution of wings

General patterns from the fossil record •  Oldest hexapods date from the Lower Devonian (395 mya). Oldest

winged insects date from the Lower to Mid Carboniferous (325 mya). There is a gap of about 55 million years between these two dates in during which no apterygote, pterygote or transitional forms are known.

•  Less than 0.5% of extant hexapods are primitively wingless (entognathans and apterygotes).

•  No modern or fossil adult insects have “rudimentary wings”. Wings are either absent or fully formed and functional.

•  First fossil entognathans and apterygotes are small in size, whereas first fossil pterygotes are very large in size.

•  Paranotal-origin theory (a). Wings are derived from rigid, lateral lobe-like expansions of the thoracic terga. Protopterygotes are derived from terrestrial ancestors.

•  Pleural-origin theory (b). Wings are derived from articulated lateral extensions from the pleuron in the form of modified gills, styli or exites. Protopterygotes are derived from aquatic ancestors.

Two competing theories for the anatomical origin of wings

From Grimaldi & Engel (2005)

Paranotal-origin theory •  Wings had their origin as rigid lateral lobes of

the thoracic terga that functioned in mating, protection or thermoregulation. Lobes eventually co-opted for use in parachuting descent initially and after further modification in gliding and full flapping flight. A hinge or flexible articulation evolved during the transition from parachuting to gliding.

•  Evidence in favor of this theory. Paranotal lobes common in arthropods, including apterygotes. Tracheation patterns in wings is similar to the pattern in the lateral lobes of some insects. Rigid paranotal lobes in some insects may be moved through deformation of the thorax by using indirect muscle attachments as seen in extant insects.

•  Evidence against this theory. Evolution of a fully articulated joint for the wings independent of other appendages is unlikely. Reconstruction of extinct

Paleodictyopteridan with paranotal lobes. From (Grimaldi & Engel 2005)

•  Wings had their origin as articulated flaps that extend from the pleural region of the thorax. The most recent version of this theory argues that the wings originated from a wing exite that occurred on the first segment of protoarthropodean leg (the epicoxa). Original function of this exite may have been respiratory (moving water past the gills of aquatic insect nymphs) and/or locomotory (as oars in the water or for skimming across the water surface).

•  Evidence in favor of this theory. Exite already has a flexible articulation with the thorax, so there is no need to evolve one. Some basal groups of insects (e.g., the Plecoptera) use their wings to skim across the water surface. Neontological studies suggest leg-related structures are involved in wing ontogeny. Neurological and muscular connections of wings are similar and overlapping with those of legs.

•  Evidence against this theory. No evidence that protopterygotes evolved from aquatic ancestors.

Pleural-origin theories

Functional shifts and the evolution of wings •  Regardless of whether wings evolved from

paranotal lobes or pleural exites, protowing structures must have undergone a functional shift from their original function to their new function in flight. How did this function shift occur?

•  Using experimental models, Kingsolver & Keohl (1985) investigated a functional shift in protowings from thermoregulation to flight.

•  Short wings have large thermoregulatory effects relative to wingless model, but this effect is larger in smaller models than in larger ones. Large wings do not significantly increase thermoregulatory effects relative to short wings. This means thermoregulatory effects cannot promote protowing extension.

Functional shifts and the evolution of wings •  Short wings have no significant effects on any

aerodynamic properties relative to wingless models in small model, but they do in large model. Large wings have significant effects on aerodynamic properties and these effects are larger in larger models than they are in smaller insects. This means that insects of larger body size benefit aerodynamically from an increase in protowing length and insects of smaller body size do not.

•  Kingsolver & Keohl argued that protowings initially served a thermoregulatory function and that function shifted toward a gliding/flying function as the average body size of insects increased early in their evolution.

•  The transition from thermoregulatory function to flying function was facilitated by scaling effects in the balance between these two functions. The shift from thermoregulatory advantage to aerodynamic advantage occurred at relatively shorter wing spans in larger insects.

What promoted the increase in insect body size at the time of origin of pterygotes (the Early Carboniferous)?

Origin of wings and gigantism •  The earliest pterygotes in the Carboniferous

were extremely large in body size. Wingspans of the Protodonata exceeded 70 cm in one species. Wingspans of the Paleodictyoptera ranged from 0.9 to 43 cm. Gigantism was widespread in both winged and non-winged hexapods of the late Paleozoic.

•  Atmospheric concentration of O2 increased rapidly in Early Carboniferous, while CO2 dropped. This increase in O2 occurred without a drop in N2, thus increasing the density of the atmosphere.

•  Increased O2 and air density allowed insects to increase in size because it enhanced the diffusion of O2 through the tracheae. Higher air density also enhanced the aerodynamic properties of any protowings and promoted an increase in length. This hypothesis explains the correlation between insect gigantism and the origin of wings.

Summary •  Insects evolved wings some time before 325 mya. They

problably first appeared in large insects during the Carboniferous period when oxygen concentrations were high.

•  Structures that gave rise to wings may have been rigid extensions on the dorsum of the thorax (protonal theory) or flexible extensions on the plural side of the thorax.

•  Protowings served another (thermoregulatory?) function before they functioned as wings. The functional shift to flight may have occurred as insects increased in size during the Carboniferous period.

•  Large flying insects became extinct during the Permian period due to a decrease in oxygen concentration.

Gliding in Wingless Ants Cephalotes atratus

Gliding in Wingless Ants Camponotus heathi

Gliding in Wingless Ants

Some stoneflies use their wings to row or skim across the water