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Small, fast…yet still in control ! how insect flight deals with the challenge of

miniaturizationSanjay P. Sane

National Centre for Biological SciencesTata Institute of Fundamental Research

Bangalore, INDIAsane@ncbs.res.in

Musca Domestica (wing beat frequency = 200-250 Hz)2

Insect flight involves parallel and hierarchical activesensorimotor processes

Musca domestica,2000 fps

Insect flight involves parallel and hierarchical activesensorimotor processes

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How do insects fly?

MigrationMoth and butterfly migrations in Panama,Peninsular India and Australia

Aerodynamics of flexible wings.

Biological effects of induced flow ininsects.

How do insects fly?

Search behaviorDrosophila

visual-olfactory integration.

Antennal control of flight (moths and bees).

Haltere control of flightin soldier flies.

Rapid turns, take-off and landing in Musca.

Wing-wing and haltere-wing coordination in flies.

SensorimotorNeurobiology

Musculo-skeletal mechanics

Aerodynamics

Other projectsMechanics of prey capture In Utricularia.Termite Mound Architecture

Moth- Plant Interactions

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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

One of smallest insectsMegaphragma mymaripenne 4600 Neurons, Anucleate!Smaller than Paramecium(wing span ~ 0.04 cm)

Polilov, Nature 2011

Largest extant insect:Queen Alexandra’s Bird wing(wing span ~30 cm)

O+

The largest insect ever found:

Meganeurid dragonfly (extinct)

From the Carboniferous period

~300 Million years ago(wing span ~ 65 cm)

Miniature videos

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Deora, Gundiah and Sane (2017), in press is constrained, so as R decreases n must increase to compensate

Smaller insects must enhance wing beat frequency to generate sufficient aerodynamic forces for flight

= 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

Flight Force = 0.5 CL,D U2 SU=2n R

S=c R , where c ~RFlight Force = 2CL,D 2 n2R3c

Flight Force ~ 2 n2R4

but Mass ~R3

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Deora, Gundiah and Sane (2017), in press; adapted from Dudley (2000) and Wilson (1972)Miniaturization occurred independently in every insect clade

Smaller insects must enhance wing beat frequency to generate sufficient aerodynamic forces for flight

Flight Force = 0.5CL,D U2SU=2n R

S=cR , where c ~RFlight 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

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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.

Pringle (1949); Roeder (1951) ; Josephson (2000)

Wing movement

Muscle activity

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Delayed stretch activation in indirect flight muscles

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Indirect flight muscle architecture

Indirect Flight Muscles

Deora, Gundiah and Sane, J Exp Biol (in press)

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38%

13%16%

13% Hyperdiverse orders

Myogenic muscle + Indirect Flight Muscle Architecture correlate with diversity

Orders with myogenic+IFM architecture

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Indirect flight muscles cause resonant contractions of the thorax

Deora, Gundiah and Sane, J Exp Biol (in press)

Direct Steering Muscles

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The main questionsFlight-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?

Tanvi Deora Deora, Singh and Sane, PNAS 2015

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Halteres oscillate anti-phase to wings

Wing beat frequency ~ 100 Hz, filmed at 2000fps

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Halteres provide crucial mechanosensory input for flight control in Diptera

The base of the haltere is covered with fields of campaniform sensillawhich transduce strain information to the flight control system

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Sherman & Dickinson, J. Exp. Biol. (2003) Chan, Prete & Dickinson, Science (1996)

Halteres detect gyroscopic forces in Diptera

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Normal

Left Haltere ablated Right Haltere ablated

Both Halteres ablated

Haltere ablation affects ipsilateral wing

Kumarvardhanam Daga

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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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Mechanical Coupling

Neural Coordination

How do wings and halteres maintain a precise phase relationship?

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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

(Redrawn from M. Demerec (1994))

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A video summary of the wing hingemechanism

Wing hinge alters configuration to change kinematics

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A mechanical model for haltere-wing coordination

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Wings and halteres are weakly coupled, independently driven oscillators synchronized by linkages of finite stiffness

Deora, Singh and Sane, PNAS (2015)

Ensures robustness in face of wing damage

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The neural basis of clutch coordination in flies

Sadaf, Reddy, Sane and Hasan, Current Biology (2015)

Gaiti Hasan

Sufia Sadaf

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Direct flight muscle architecture

Deora, Gundiah and Sane, J Exp Biol (in press)

Direct Steering Muscles

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Tanvi Deora, NCBS

Dr. Namrata GundiahMechanical Engineering

IISc

Shilpa Naik, BITS Pilani

Nehal Johri, St Xavier’s College,Mumbai

Amit Singh, NCBS

Abin GhoshNCBS

Akash Vardhan, NCBS

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Disengaged vs Engaged thorax

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Reconstituting behaviors in the lab: Landing

Musca domestica (3000 fps, wing beat frequency= 250 Hz)Sathish Kumar, Rana Kundu, Navish Wadhwa

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Assaying complex behaviors…

Pranav Khandelwal, Sam Wallis, Tanvi Deora Sathish Kumar

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R. Dudley (UC Berkeley)Robert Srygley (USDA)

SensorimotorNeurobiology

A. Krishnan,S. SudarsanS. Prabhakar

Taruni RoyJ. Subramanian

Rana Kundu Sathish KumarUmesh MohanHarshada Sant Payel Chaterjee

Maitri HegdeDinesh Natesan

Musculo-skeletal mechanics

AerodynamicsX. Deng (Purdue)

Bo Cheng (UPenn )Yun Liu

Jesse RollBixing

How do insects fly?

Search behaviorNitesh Saxena Aravin Chakravarty

Gaiti Hasan (NCBS)Namrata Gundiah

(IISc)Sufia SadafTanvi DeoraShilpa NaikAbin Ghosh

Akash Vardhan

NCBS, SIDA,AOARD, AFOSR, ITC-PacificRamanujan, NDRF

HFSP

Amit Singh(Utricularia, Ajinkya DahakeKemparaju, Deepak(Moth biodiversity)

FUNDS

Modular behaviorsNavish WadhwaTejas CanchiVardhanam Daga

Amritansh VatsParmeshwar PrasadSreekrishna VarmaRaja(Termite mounds)

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Indirect flight muscle evolution

Deora, Gundiah and Sane, J Exp Biol (in press)

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