Download Bio5445 Lecture 13 - Biology Courses Server

Flight II: Evolution of Wings and Flight
Major questions concerning the evolution of wings
•  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?
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.
Two competing theories for the
anatomical origin of wings
•  Paranotal-origin theory (a). Wings
are derived from rigid, lateral lobelike 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.
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)
Pleural-origin theories
•  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.
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