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IF NATURE is red in tooth and claw, then what about the green bits? Animals
may fight to the death but surely plants are more benign. They make a good
subject for a still life and can even inspire poetic passions, but they couldn’t
possibly have aggressive tendencies. Or could they?

According to a new breed of botanists, inside delicate flowers and luscious
fruits lurk conflicts of interest as unforgiving as any in the animal kingdom.
Plants may not have brains or even a nerve cell between them, but they still
behave selfishly. And those researchers who have cast aside their neurocentric
prejudices are finding that the family life of plants is more tempestuous than
anyone suspected. In fact, evolutionary theories designed to explain animal
behaviours such as mate choice, offspring greed and sibling rivalry are just as
enlightening when applied to plants.

Flowering plants are symbols of passive beauty. Rutting stags may clash
antlers over females and skuas may kill sexual rivals, but floral fertilisation
is often seen as more a matter of luck. Pollen carried by a capricious breeze or
at the whim of an insect arrives at the female flower, and parents wed their
genetic fates by producing seeds that, in turn, are carried wherever the winds
or the vagaries of a hungry vertebrate’s wanderings may take them. But even
before self-respecting botanists dared speak seriously of plant mating
behaviour, germination experts realised that fertilisation is not random. Some
pollen donors have a considerable reproductive advantage over their competitors,
fathering more than their fair share of the seeds a female produces. How this
happened was a mystery, however, until Diane Marshall from the University of New
Mexico in Albuquerque decided to investigate.

Marshall, a pioneer of plant behaviour research, began looking for evidence
of direct competition between pollen grains over a decade ago. The idea that
sperm from different males compete inside a female animal’s reproductive tract
is now taken for granted. Researchers have even found chemicals in the semen of
male fruit flies that destroy the sperm of competitors. Marshall suspected that
reproductive striving between plants could be equally intense. In that case, the
race to fertilise each egg could be won by more than mere speed as pollen tube
cells burrowed their way through female tissue towards the ovary.

Pugilistic pollen

To test this idea, Marshall and her students pollinated wild radishes by hand
to see whether there was a difference between those that received pollen from a
single source and those pollinated by more than one other flower. And sure
enough, when there was competition between pollen, germination rates fell. A
closer look revealed that this occurred only when grains from different males
actually touched each other. In other words, pollen grains somehow inhibit the
growth of their competitors, preventing them from successfully growing a pollen
tube to take the male reproductive cells down the flower to the ovule where the
ovary sits (see Diagram).
Now Emilie Miller, a student in Marshall’s lab,
is investigating the chemical basis of interference competition among tubes, a
process known as allelopathy. “Allelopathy among pollen grains of different
species is known,” says Marshall. A similar chemical assault may explain her
findings for competition between pollen of a single species, as well. “I am
betting that the effect is chemical,” she adds.

But is nonrandom mating in plants strictly a matter of male combat, or might
female plants somehow sort through pollen and select genetically superior grains
to sire their young? The Darwinian logic is clear: if more pollen is available
than females need just to reproduce and the quality of potential fathers varies,
then mechanisms that allow a female to choose between males should evolve. Stare
a daisy in the petals, though, and it seems hard to believe. Mate choice implies
a consciousness obviously absent from these organisms, but that hasn’t stopped
the sociobotanists looking for it—and with some success.

A few years ago, Mitchell Cruzan, then at the State University of New York at
Stony Brook, found that in one species of petunia at least, females do
discriminate among pollen grains in their styles—the plant equivalent of
the reproductive tract. Cruzan pollinated immature flower buds and the styles of
mature flowers, and found that fewer of the pollen germinated inside the fully
developed plants than in the immature ones. If pollen vigour alone explains
variation in male mating success, then germination rates should have been the
same. He concluded that immature buds are less able than mature flowers to
inhibit the growth of tubes from second-rate pollen.

Marshall, too, has found that pollen sorting occurs in the styles of wild
radishes. Her experiments, like Cruzan’s, reveal that immature styles are less
discriminating, with the result that mating is more random than in mature
flowers. In many species, the style exudes a chemical trail that guides pollen
tube growth. This may be the mechanism for female control of germination.

But if pollen sorting really is sexual selection in action, then the mating
preferences of unrelated females must agree. If some females prefer the pollen
of one male but others prefer that of another, sorting may be nothing more than
a way to prevent inbreeding with close relatives. Using her wild radishes,
Marshall has just tested this crucial prediction and reports that there is
indeed significant agreement in the choice of mates made by unrelated females.
The number of seeds sired by each pollen donor is remarkably consistent,
providing yet another challenge to the still prevailing presumptions that floral
reproduction is a passive process.

Moreover, sexual rivalry is not the only behavioural trait that plants seem
to share with animals. Nearly 25 years ago, evolutionary biologist Robert
Trivers first proposed the idea of parent-offspring conflict. He pointed out
that in sexually reproducing species, young are only half related to their
mothers, and that this difference in genetic self-interest should result in the
evolution of a mismatch in survival strategies between parents and their
offspring. In other words, an offspring demands more from its parents than they
can afford to give it.

Trivers was trying to explain animal behaviour, but even then other
evolutionary theorists, such as William Hamilton of the University of Oxford,
pointed out that natural and sexual selection should result in similar
competitive strategies regardless of whether genes are carried in a furry or a
flowered package. Now R. Uma Shaanker, K. N. Ganeshaiah and their colleagues at
the University of Agricultural Sciences in Bangalore, India, are showing that
theories of animal behaviour do indeed extend to plants.

Parent-offspring conflict is one of those ideas that seems obvious when
someone points it out, but it has proved to be anything but a trivial truism.
For example, David Haig of the Museum of Comparative Zoology at Harvard
University found that human embryos produce hormones that manipulate the
structure of placental blood vessel, maternal blood pressure and blood sugar
levels to increase the nutritional input they get in the womb. Not only that,
but mothers have evolved counter-strategies, using their own hormones, to combat
this fetal exploitation.

When Uma Shaanker and Ganeshaiah began their work two decades ago, the idea
that plants might be engaged in similar battles encountered outright hostility.
Undaunted, they pursued their heresies, even using provocative zoological terms
such as “dominance”, “clutches” and “broods” to describe what they found. Seeds
are not fed by the plant equivalent of blood vessels, the phloem. Instead,
nutrients flow directly from the adjacent maternal fruit tissue. So, working
with K. V. Ravishankar, the researchers reviewed the botanical literature
looking for hormonal interactions between seeds and fruit. What they found
convinced them that the hormonal tug of war between human embryos and mothers
described by Haig was also being fought out in plants. Offspring tissues
synthesise hormones such as gibberellic acid and indole acetic acid (auxin) that
take nutrients from maternal tissues, while tissues under maternal control, such
as the seed coat, produce abscisic acid, which curbs offspring’s appetites.

Putting hormonal interactions in the context of family conflict also seems to
clear up a long-standing mystery of germination physiology. Maternal abscisic
acid production peaks twice during embryo development. The second
peak—shortly before seeds leave the fruit to fend for themselves—
imparts drought tolerance to seeds. But the function of the earlier peak has
eluded researchers. The Indian team argues that the first peak’s timing, which
coincides with offspring production of auxins and gibberellic acid, suggests
that it is the maternal response to the indiscriminate nutritional greed of
growing seeds.

Parents are not the only target for an offspring’s selfish tendencies.
Trivers’s theory also predicted rivalry between siblings—which share only
half their genes on average. In birds such as boobies and many raptors, older
chicks kill their weaker siblings, a pattern of behaviour called “obligate brood
reduction”. Uma Shaanker and Ganeshaiah believe that obligate brood reduction
may explain why in many species of plants, multiple fertilisations lead to only
a single or a very few seeds. “Seeds developing in close physical and temporal
proximity in a fruit,” they say, “can be expected to interact as intensively
among themselves as fledglings developing in the nest of a bird.”

The team has found that in several species where fruits are dispersed as a
unit by animals, wind or water, the efficiency of this process and the survival
chances of each seed decreases the more seeds there are in a single fruit. So in
most fleshy fruits, such as plums, blueberries and raspberries, natural
selection should favour seeds that can reduce fruit crowding by their siblings,
because these are the ones more likely to grow to maturity. In the black plum,
at least, this seems to be the case. Each flower has about 30 ovules, yet there
is only one seed inside the mature fruit. In a recent study, Ganeshaiah prepared
solutions of ground-up first-fertilised “dominant” seeds and pulverised maternal
plant tissue. Applying these to recently fertilised ovules, he found that
exposure to the dominant seeds’ remains prevented the uptake of sucrose,
starving the baby seeds. Not so for maternal tissue mixtures. Thus sibling
rivalry rather than maternal pruning accounts for seed death in these plums.

If normal siblings with half their genes in common compete, then the rivalry
between more distantly related offspring should be even greater. So the Indian
researchers were not surprised to find that in several flowering plants,
pollination by multiple sires results in a higher incidence of seed abortion in
a brood and in greater average seed weights among the surviving offspring. In
wild radish and mustard, for example, fratricide seems to be rife. So where are
the parental counter-strategies to reduce death rates among the offspring they
have invested in?

Uma Shaanker suspected that plant mothers might be exerting some control
through the endosperm, the plant equivalent of an egg yolk. Endosperm cells
contain two copies of the mother’s chromosomes but only a single set of paternal
genes, donated by the pollen. This so-called triploidy is a major enigma in
germination biology. If it evolved as a maternal strategy for keeping offspring
in check, Uma Shaanker reasoned, then endosperm should be found more often in
species with several ovules—where sibling rivalry is likely to
occur—than in those with a single ovule. Moreover, species with
well-developed endosperm should have lower rates of seed loss caused by sibling
murder.

In a review of over a thousand species of plants, Uma Shaanker’s team found
that in species where the endosperm is less well developed, such as orchids,
legumes and wild radish, there is indeed a high incidence of seed abortion.
Moreover, species with several ovules, such as the castor-oil plant and maize,
tend to have a better developed endosperm than those with only one. “The
evolution of triploid endosperm,” Uma Shaanker and Ganeshaiah concluded in a
recent paper, may indeed represent a maternal adaptation for “maintaining a more
equitable allocation of resources among siblings”.

Some researchers remain sceptical about the idea of family conflict in
plants. Brenda Casper of the University of Pennsylvania in Philadelphia believes
there is often no real conflict between seeds and their parents. Brood reduction
may not always hurt maternal fitness, she points out, as “fewer but larger seeds
might actually generate more successful offspring than many, smaller seeds”.
Casper has found that in neotropical flora, single-seededness is closely related
to the design of the fruit. Indehiscent fruits such as mangoes, which do not
open to release their seeds, are more likely to produce a single seed. She
argues that as fruits are maternal tissue, single-seededness is likely to be
under maternal control. If sibling rivalry plays an important role, then why
aren’t there more examples of ovule abortion leading to single-seededness in
fruits that open, she asks.

Vegetables can be beastly

Even so, Casper is not totally opposed to the idea of sociobotany. “Applying
sociobiological concepts such as parent-offspring conflict to plants speeds
progress in the field of plant reproductive ecology,” she comments, “even if the
theoretical approaches are eventually proven incorrect.” Indeed, she accepts
that sexual selection is occurring in plants.

Marshall, Ganeshaiah, Uma Shaanker and the other sociobotanists are confident
in their approach. “Though plants can neither sing nor dance,” wrote the Indian
researchers in a recent paper, “they do indulge in sibling rivalry, fratricide
and kin cooperation as intensely as animals do.” Other biologists seem to be
warming to the overall message. Trivers, now at Rutgers University, notes with
irony that his ideas, once criticised as being “highly anthropomorphic”, have
gained wider acceptance in the plant sciences and among geneticists than in
mainstream psychology or the social sciences.