Everything old is new again

6 September 2013 by Malcolm Campbell, posted in Biology

Don't throw the past away, You might need it some rainy day, Dreams can come true again, When everything old is new again." from Everything Old Is New Again by Peter Allen (1944-1992).

Remarkable innovation greets us every day. Here, in the waning days of summer, the last of the season’s flowers serve as a stage – showcasing innovation that had evaded our understanding until relatively recently.

A variety of bees make their way from flower to flower, gathering nectar and pollen. Laden with these treasures, they return to their nests to provide nourishment to those that wait there. While there is much to admire about all aspects of this mission, it is the transit from flower to flower, and flower to nest, that is truly a wonder of nature.

The mechanisms underpinning bee flight have been a perplexing conundrum for the better part of a century. In his 1934 treatise on insect flight, Antoine Magnan revealed that his colleague André Sainte-Laguë had calculated that bee flight was an aerodynamic impossibility.  Bee bodies, especially bumblebee bodies, were simply too large to be compensated by the haphazard nature of winged flight. And yet they flew. How was this possible?

Using high-speed digital photography, Altschuler, Dickinson and colleagues found that bees exploit a combination of exotic mechanisms to sustain flight. They use an unconventional mix of short, choppy wing strokes, a rapid rotation of the wing as it flops over and reverses direction, and a very fast wing-beat frequency.

Bee wing-beat frequency is itself extraordinary.

As aerodynamic performance decreases as insects get smaller, normally it is the smallest insects that flap their wings at the most furious rates. For example, mosquitoes flap their wings at a rate of 400 beats per second. That’s right, per second!

Fruit flies might be a better comparison for bees, because their body shapes are more similar.  Fruit flies are 80 times smaller than honey bees, and beat their wings at 200 beats per second. Compare this to the much larger honeybee, which can beat its wings at an astonishing 230 beats per second.

When bees make their way from their nests, unburdened by pollen or nectar, they achieve their rapid wing beats by flapping them through a very short arc, only about 90 degrees. On their way back to the nest, carrying their floral-derived bounty, one would anticipate that the bees would increase their wing-beat frequency, to keep themselves aloft. Surprisingly, laden bees don’t increase their wing-beat frequency. Instead, they sustain the same wing-beat frequency but increase the arc of their wing strokes.  This is a curious solution to contend with flying with a payload, as it would be aerodynamically more efficient to flap faster. There must be something about the bee flight muscles that make this a useful manner to fly.

Bee wings are powered by flight muscles. Interestingly, bee flight muscles share the same basic features of your skeletal and cardiac muscles. These basic features include the three key types of protein that enable muscle to do work through contraction. Muscle contains long filaments of a protein known as actin. Actin filaments function as tethers for muscle contraction – like ropes that one is going to pull on to bring one end of the muscle closer to the other. The protein that does the pulling is myosin.

Like actin, myosin has a tether-like region. This is at its tail. At its head, myosin has a “motor protein” function. The myosin head has an affinity for actin. When it binds to actin, the myosin head group is pulled towards the tail by kinking at a neck-like region.

You can mimic the action of myosin on actin by stretching out your arm straight, palm downward, with a fist at the end. Your arm is the myosin tail, and your fist is its head. Reach out with your knuckles to piece of paper on a table. While an imperfect representation, we’re going to pretend that the paper is an actin filament. When your knuckles come into contact with the paper, bend your wrist so that your knuckles curl towards your forearm. This should move the paper towards you. That, in the broadest terms is how myosin and actin work together.

In relaxed muscle, actin is masked from myosin by another type of proteins called troponins. When you want to contract a muscle, you transmit a signal from motor nerves to the muscle. This signal causes calcium ions to be released within the muscle. Troponins bind the calcium, and enable the actin filaments to rotate and expose mysosin-binding sites. Myosin head groups then bind the exposed actin, and pull the filaments toward the ends of the muscle, thereby creating contraction.

This mechanism is great for the relatively slow, methodical movements of skeletal muscle, and even for the faster contractions that take place in cardiac muscle, but it is no good for the rapid action of bee flight muscle. Bee flight muscle needs to contract much more rapidly than the release and re-uptake of calcium would allow. What’s more, the energetic costs of the human muscle contraction mechanism are just too high to enable the hundreds of contractions in a second that bees need.

How do bees make use of the same basic structure as vertebrate muscle to accomplish a much more demanding task?

Bee muscles oscillate spontaneously after they have been activated. They do this through a process called “stretch activation”. In stretch activation, force is generated by two, out-of-phase, antagonistic flight muscles.  This force gets stronger as the flight muscles are extended, which pulls the wing back.

Until recently, it was not know how stretch activation really worked. It could arise from a simple mechanism – one that just involves the natural affinity of myosin for actin, where the number of head groups that can bind actin just increases as the muscle extends. Alternatively, it may be that there is a special kind of troponin that is at work – one that does not require calcium for its activation.

Very recently, Iwamoto and Yagi provided key insights into how stretch activation works in bee flight muscle. They placed live bumblebees in the path of X-rays. The scattering of these X-rays enables them to measure the activity of actin and myosin during stretch activation while the bees flapped their wings. In a technical tour de force, X-ray data were collected at a phenomenal rate – 5000 frames per second – fast enough to determine what was taking place during the high-frequency wing flapping.

Astonishingly, the data suggest that myosin heads in bee flight muscle rotate when muscle stretches, enabling them to better bind actin. That is, stretch activation is a fundamental consequence of way in which flight muscle actin and myosin interact. In essence, flight muscle is doing little different from what your skeletal and cardiac muscle do, except with one step missed out – the need for calcium fluxes during the oscillating contractions.

In essence, evolution has beautifully captured the fundamental properties of muscle and deployed them in a different contexts. One can view these fundamental properties like a module that evolution has repurposed to equip some species with novel functionality. It’s like a line of code that has been re-used in the context of a different algorithm. The code still says to do the same thing, but, in the context of the new algorithm, the overall impact of that instruction is different. The fundamental properties of muscle were laid down in a common ancestor of bees and humans. We share that common legacy, making use of that old module to do new things.

References:

Altshuler DL, Dickson WB, Vance JT, Roberts SP, & Dickinson MH (2005) Short-amplitude high-frequency wing strokes determine the aerodynamics of honeybee flight. Proceedings of the National Academy of Sciences of the United States of America, 102: 18213-18218

Iwamoto H, & Yagi N (2013) The molecular trigger for high-speed wing beats in a bee. Science (epub ahead of print)

Magnan A (1934) Le vol des insectes. Hermann.

Images: All photographs by Malcolm M. Campbell.

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