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amnhhealiz1Sex is in the Air

Birds do it. Bees do it. Sometimes even gentle breezes do it.

Story by Adam Summers - Illustrations by Sally J. Bensusan

The rugged volcanic cliffs of the Hawaiian Islands are the first obstacles encountered by the northeasterly tradewinds roaring across the Pacific Ocean. Stephen Weller, gingerly feeling his way down the steep face of a cliff, is glued to the rock by (in equal parts) the stiff breeze and a single-minded desire to collect one more species of Schiedea, a genus of plants endemic to the Hawaiian Islands. He hopes to determine the role of wind-a distinctly nonbiological process-in the evolution of that most fundamental of biological functions: reproduction.

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Male flower cluster

Female flower cluster

The complexity of plant reproduction is the bane of undergraduate biology. Lots of plants reproduce asexually, essentially cloning themselves, a method that sacrifices the advantages gained from the reshuffling of genes in sexual reproduction. In flowering plants that reproduce sexually, the analogues of sperm and eggs are, respectively, pollen and ovules, both produced within the flower. From there, things can get weird. Many plants have hermaphroditic flowers, which produce both pollen and ovules. Others have two kinds of flowers: some that produce only pollen and some that produce only ovules. In still other species, individual plants produce flowers of only one sex or the other. A flower that generates both pollen and ovules has the potential to fertilize itself, but such inbreeding can lead to a concentration of bad genes-perhaps a just reward for selfish behavior. For this reason, the architecture of most hermaphroditic flowers inhibits self-fertilization-for example, the anthers (which contain the pollen) will not be situated too close to the stigma (the upper part of the style, a stalklike structure that leads to the ovary). This increases the likelihood that pollen will be carried out of the flower, often by insects, birds, or bats, and be deposited somewhere far from home.

Anyone with spring allergies, however, is all too aware that many plants rely not on animals for pollination but on the wind. The drawback to this approach is that while a butterfly may flit from blossom to blossom in search of nectar, thereby boosting the chances that it will deliver pollen from one plant to another, a breeze has no destination in mind. A given pollen grain blowing in the wind is thus unlikely to land on a receptive stigma. To compensate, plants that are pollinated by the wind tend to produce lots and lots of pollen (often, tens of thousands of grains per flower). That coating of yellow powder on cars in the springtime is a testament to the number of grains needed to make up for the very remote chance of a meeting between male and female gametes.

But how to get the beautifully sculptured spheroids of pollen off the anther and into the air? This is not so simple a proposition as it might sound. Pollen grains are tiny: it would take two large ones, or about forty-five small ones, just to span the period at the end of this sentence. Pollen is, in fact, so small that it hides within the boundary layer, a film of air that remains still even on swiftly moving surfaces. (You may have noticed that dust builds up on the blades of ceiling fans. Even if the fan is never turned off, dust collects in the boundary layer, where the wind is not strong enough to move it.) To make sure that pollen gets scattered, the anthers of wind-pollinated flowers are built to shake and shimmy in the breeze.

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Like many wind-pollinated species, Hawaii's cliff-dwelling Schiedea globosa plants can be male or female. Pollen-bearing anthers stick out from the multitude of tiny flowers clustered on the male plants, while proturuding, elongate styles on the flowers of female plants capture the pollen. This separation of the sexes keeps a plant from fertilizing itself.

Once airborne, pollen grains run the risk of sailing right past a suitable landing zone. Not coincidentally, the flowers of wind-pollinated plants are usually arranged in tight bunches that block the wind, creating eddies that increase the odds of successful pollen delivery. In some cases, the clustering of flowers actually serves as an aerodynamic sieve, helping ensure that only pollen grains of the appropriate size settle onto the stigma.

For a plant morphologist, a quick look at the level of pollen production and the shape and distribution of the flowers and floral parts is usually enough to tell whether a plant is pollinated by wind or by animals. Sometimes, however, morphological information is not enough. The issue can then be settled with an empirical, biomechanical test. In a large wind tunnel (the kind used for testing airfoils), plants are arranged in small groups so that the flow of air around them mimics the airflow in nature. The wind speed in the tunnel is varied, from the light breezes that might blow across a quiet valley floor to the near gales that frequently batter an exposed ridge. Airborne particles are collected on sticky microscope slides placed downwind of the plants. The farther pollen rides the artificial gusts, the more likely it belongs to a wind-pollinated plant.

The Schiedea that Stephen Weller was risking life and limb to collect grow on windy cliffs, but members of the genus can be found in just about every conceivable habitat, from forests (where the genus originated) to valleys and open country. Lusher than their wind-blasted cousins, the forest-dwelling species display flowers that are clearly pollinated by insects. But it would take a powerful insect, or a very brave bird, to pollinate the plants that cling to exposed slopes, consistently buffeted by thirty-mile-an-hour winds. As you might expect, the flowers on these plants have the shape and pollen count associated with the breezy mode of pollination.

Weller, together with his colleague Ann Sakai (both of whom are at the University of California, Irvine), noticed that wind-pollinated Schiedea species have flowers of a single sex, while insect-pollinated ones have hermaphroditic flowers. Plants that rely on the wind and that produce both prodigious amounts of pollen and flowers adapted to catch it, they reasoned, would be especially prone to "inbreeding depression" (when inbred offspring don't reproduce as well as individuals whose parents are less closely related) if their flowers were hermaphroditic. Could wind, with its quixotic eddies, drive the separation of male and female aspects of reproduction?

Having determined the pollination method of more than a dozen species based on anatomy alone, the researchers tested the rest inside the wind tunnel-running the tests in the evening because that is when the anthers release their pollen. When Weller and Sakai checked the slides for pollen, the answer was clear: Species of Schiedea that had moved from the forest into dry, windy habitats had evolved wind-pollinated flowers with separate male and female reproductive systems. In these plants, the answer to the question of whether their flowers can pollinate themselves is blowin' in the wind.

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