Download Small, fast…yet still in control !

Small, fast…yet still in control !
how insect flight deals with the challenge of
miniaturization
Sanjay P. Sane
National Centre for Biological Sciences
Tata Institute of Fundamental Research
Bangalore, INDIA
[email protected]
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Insect flight involves parallel and hierarchical active
sensorimotor processes
Musca Domestica (wing beat frequency = 200-250 Hz)
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Insect flight involves parallel and hierarchical active
sensorimotor processes
Musca
domestica,
2000 fps
How do insects fly?
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How do insects fly?
Musculo-skeletal mechanics
Wing-wing and halterewing coordination in flies.
Aerodynamics
Aerodynamics of
flexible wings.
Biological effects
of induced flow in
insects.
Sensorimotor
Neurobiology
Antennal control of
flight (moths and bees).
Haltere control of flight
in soldier flies.
Rapid turns, take-off and
landing in Musca.
Other projects
Mechanics of prey capture
In Utricularia.
Termite Mound Architecture
Migration
Moth and butterfly
migrations in Panama,
Peninsular India and
Australia
Search behavior
Drosophila
visual-olfactory
integration.
Moth- Plant
Interactions
Insects: an evolutionary success story
Estimated 6-10 million species (>1 million
already described!)
>90% of all multicellular animals
Flying insects range in size scales spanning 3
orders of magnitude
Occupy vast variety of ecological niches
First fossils from ~ 400 Mya (early Devonian)
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Miniaturization of body size and evolution of flight
The largest insect
ever found:
O+
Meganeurid dragonfly
(extinct)
From the Carboniferous
period
~300 Million years ago
(wing span ~ 65 cm)
Largest extant insect:
Queen Alexandra’s
Bird wing
(wing span ~30 cm)
One of smallest insects
Megaphragma mymaripenne
4600 Neurons, Anucleate!
Smaller than Paramecium
(wing span ~ 0.04 cm)
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Polilov, Nature 2011
Miniature videos
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Smaller insects must enhance wing beat frequency to
generate sufficient aerodynamic forces for flight
Flight Force = 0.5 CL,D U2 S
U=2n R
S=c R , where c ~R
Flight Force = 2CL,D 2 n2R3c
Flight Force ~ 2 n2R4
but Mass ~R3
 = Density of medium
U = Linear velocity of wing
S = Projected surface area of wing
CL, D= Coefficient of Lift or Drag
= Angular amplitude
n = wing beat frequency
c= chord length, R = wing length
 is constrained, so as R decreases n must increase to compensate
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Deora, Gundiah and Sane (2017), in press
Smaller insects must enhance wing beat frequency to
generate sufficient aerodynamic forces for flight
Flight Force = 0.5CL,D U2S
U=2n R
S=cR , where c ~R
Flight Force = 2CL,D 2 n2R3c
Flight Force ~ 2 n2R4
but Mass ~R3
 = Density of medium
U = Linear velocity of wing
S = Projected surface area of wing
CL, D= Coefficient of Lift or Drag
= Angular amplitude
n = wing beat frequency
c= chord length, R = wing length
Miniaturization occurred independently in every insect clade
Deora, Gundiah and Sane (2017), in press; adapted from Dudley (2000) and Wilson (1972)
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How do insects cope with smaller body size
and greater wing beat frequency?
1. Sensory systems need to sample with high temporal
resolution.
2. Motor system needs to be faster and more accurate.
3. Energy losses must be minimized through elastic storage
etc.
4. Water losses must be compensated.
etc.
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The evolution of myogenic (or asynchronous)
flight muscles
Dipteran wings beat at frequencies of the order of 100 Hz or higher, a rate
which is not possible by direct neural stimulation.
Myogenic muscles can have multiple contraction cycles per neural
stimulation.
Wing
movement
Muscle
activity
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Pringle (1949); Roeder (1951) ; Josephson (2000)
Delayed stretch activation in indirect flight muscles
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Indirect flight muscle architecture
Indirect Flight Muscles
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Deora, Gundiah and Sane, J Exp Biol (in press)
Myogenic muscle + Indirect Flight Muscle Architecture
correlate with diversity
Orders with myogenic
+IFM architecture
38%
13%
16%
13%
Hyperdiverse
orders
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Indirect flight muscles cause resonant contractions
of the thorax
Direct Steering Muscles
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Deora, Gundiah and Sane, J Exp Biol (in press)
The main questions
Flight-control related behaviors need to be fast, often
pushing the limits of the neuronal response.
These behaviors need to be precise because small errors
can lead to large deviations from intended course.
How are insects able to achieve speed and precision
during flight control?
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Tanvi Deora
Deora, Singh and Sane, PNAS 2015
Halteres oscillate anti-phase to wings
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Wing beat frequency ~ 100 Hz, filmed at 2000fps
Halteres provide crucial mechanosensory input for
flight control in Diptera
The base of the haltere is covered with fields of campaniform sensilla
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which transduce strain information to the flight control system
Halteres detect gyroscopic forces in Diptera
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Sherman & Dickinson, J. Exp. Biol. (2003)
Chan, Prete & Dickinson, Science (1996)
Haltere ablation affects ipsilateral wing
Normal
Left Haltere ablated
Both Halteres ablated
Right Haltere ablated
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Kumarvardhanam Daga
Halteres oscillate anti-phase to wings
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How do wings and halteres maintain a precise
phase relationship?
Neural Coordination
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How do wings and halteres maintain a precise
phase relationship?
Neural Coordination
Mechanical Coupling
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The dead bug experiments
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Key mechanical coupling elements
Dorsal view of the thorax
Side view of the thorax
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(Redrawn from M. Demerec (1994))
Wing hinge alters configuration to change kinematics
A video summary of the wing hinge
mechanism
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A mechanical model for haltere-wing coordination
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Deora, Singh and Sane, PNAS (2015)
Wings and halteres are weakly coupled, independently driven
oscillators synchronized by linkages of finite stiffness
Ensures robustness in face of wing damage
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Deora, Singh and Sane, PNAS (2015)
The neural basis of clutch coordination in flies
Gaiti Hasan
Sufia Sadaf
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Sadaf, Reddy, Sane and Hasan, Current Biology (2015)
Direct flight muscle architecture
Direct Steering Muscles
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Deora, Gundiah and Sane, J Exp Biol (in press)
Tanvi Deora,
NCBS
Nehal Johri,
St Xavier’s College,
Mumbai
Dr. Namrata Gundiah
Mechanical Engineering
IISc
Abin Ghosh
NCBS
Akash Vardhan,
NCBS
Amit Singh,
NCBS
Shilpa Naik,
BITS Pilani
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Disengaged vs Engaged thorax
Reconstituting behaviors in the lab: Landing
Musca domestica (3000 fps, wing beat frequency= 250 Hz)
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Sathish Kumar, Rana Kundu, Navish Wadhwa
Assaying complex behaviors…
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Pranav Khandelwal, Sam Wallis, Tanvi Deora
Sathish Kumar
Gaiti Hasan (NCBS)
Namrata Gundiah
(IISc)
Sufia Sadaf
Tanvi Deora
Shilpa Naik
Abin Ghosh
Akash Vardhan
How do insects fly?
Sensorimotor
Neurobiology
Musculo-skeletal mechanics
A. Krishnan,
S. Sudarsan
S. Prabhakar
Taruni Roy
J. Subramanian
Rana Kundu
Sathish Kumar
Umesh Mohan
Harshada Sant
Payel Chaterjee
Maitri Hegde
Dinesh Natesan
Aerodynamics
X. Deng (Purdue)
Bo Cheng (UPenn )
Yun Liu
Jesse Roll
Bixing
FUNDS
NCBS, SIDA,AOARD,
AFOSR, ITC-Pacific
Ramanujan, NDRF
HFSP
Search behavior
Nitesh Saxena
Aravin Chakravarty
Amritansh Vats
Parmeshwar Prasad
Sreekrishna VarmaRaja
(Termite mounds)
Amit Singh
(Utricularia,
Ajinkya Dahake
Kemparaju, Deepak
(Moth biodiversity)
Modular behaviors
Navish Wadhwa
Tejas Canchi
Vardhanam Daga
Migration
R. Dudley (UC Berkeley)
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Robert Srygley (USDA)
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Indirect flight muscle evolution
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Deora, Gundiah and Sane, J Exp Biol (in press)
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