[Paleopsych] TLS: Gaden S. Robinson: Ant matters

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Gaden S. Robinson: Ant matters
The Times Literary Supplement, 4.7.30
http://the-tls.co.uk/archive/story.aspx?story_id=2108310&window_type=print

    Size, possessiveness and other essentials for an exuberant
    evolutionary

    PHEIDOLE IN THE NEW WORLD. A dominant, hyperdiverse ant genus. By
    Edward O. Wilson. 794pp + CD. Harvard University Press. £85.95 (US
    $125). - 0 674 00293 8

    FOR LOVE OF INSECTS. By Thomas Eisner. 448pp. Harvard University
    Press. Pounds 19.95 (US $29.95). - 0 674 01181 3

    Man has three close relatives - the chimpanzee, gorilla and
    orang-utan. Our ethnocentricity as systematists and our unease at
    contradicting the concept of man as a special creation are just two of
    the reasons behind our considering ourselves not just a separate
    species or even genus, but a family separate from our cousins. Had the
    classification of the living world been written by an ant, we would,
    all four of us, be lumped together in a single genus. The mammals and
    the birds each contain about as many species as a typical insect
    family - around five thousand. Most bugs have a host of close
    biological relatives; we have decided that we don't. And we find it
    for the most part very hard to visualize and explain the entirely
    different scale of species diversity that is encountered in the
    invertebrate world. Faced with an illustration and explanation such as
    Edward O. Wilson's Pheidole in the New World, we can only be stunned.

    "Pheidole is among the largest of all genera of plants and animals",
    says Ed Wilson, and he is right. There are very few genera with more
    than 750 species and even fewer with upwards of 1,000. Wilson
    introduces the term "hyperdiverse" in this monograph to describe such
    groups. These small ants are just a few millimetres long; they are
    predominantly soil-and litter-dwelling, but a significant number of
    species are arboreal. Most are scavengers and predators, but some are
    seed-collectors, and a few species have adopted highly specialized
    biologies, such as Pheidole titanis, a specialized predator of
    termites. The genus ranges from New England southwards into temperate
    Argentina, and from Southern Europe south to the Cape, east to the
    Pacific and through Australia and Melanesia as far as Samoa.

    Including those in the present contribution, 900 different species
    have been recognized, and Wilson suggests that a worldwide total of
    1,500 is not an unreasonable prediction, making Pheidole the planet's
    most diverse ant genus (a distinction currently held by Camponotus
    with about 930 species). Among the 624 species that are described in
    Pheidole in the New World, more than half, 337, are new to science.
    This is one-fifth of the ant species of the Americas, more than 6 per
    cent of the world's ant fauna. In the rainforest of Central America, a
    few square kilometres can be home to more than fifty species. Pheidole
    is not just diverse - it is numerically abundant in a wide range of
    habitats across the world. The sweet smell of biological success must
    be included somewhere among Pheidole's pheromones.

    Some biologists are chary of hyperdiverse genera. To monograph such
    groups is an enormous challenge. Many see them as unwieldy, and some
    insist that they should be divided into groups of a "convenient" size.
    The history of the "splitting" of hyperdiverse genera to make their
    components more "manageable" has been a history of disasters resulting
    in taxonomic mayhem. In the early 1970s, attempts were made to divide
    up the moth genus Coleophora (with about 1,200 species) and some
    eighty new genera were proposed. It took ten years to restore sanity
    and the status quo, and to repack the species of Coleophora back into
    their monogeneric box.

    Wilson, rightly, will have none of this. We should not expect the man
    who invented the word "biodiversity" to be awed by large genera. His
    arrangement of Pheidole, divided into informal species groups, is a
    pragmatic solution that will be applauded by both fellow taxonomists
    and the fieldworkers who will use his monograph. The species of
    Pheidole are too "tightly packed", morphologically, with too many
    sequential evolutionary radiations, and with too much "convergence in
    character traits between species groups" to be carved up. "Pheidole
    today is like a large diamond set on the bench mount of a gem cutter.
    To cleave it before seeing into its interior could be disastrous."

    Pheidole is the product of "an exuberance of evolution". Wilson's
    monograph is the product of a master craftsman. It reeks of authority.
    Opening sections explain anatomy, terminology and abbreviations. There
    are 100 pages of keys. Each one page species treatment includes line
    drawings of the major and minor workers in lateral view, frontal views
    of the heads, and details of the thorax and petiole; the location of
    the type-specimens; the derivation of the name; diagnosis,
    measurements, colour, geographical range and biology. Here are 624
    treatments - a gigantic undertaking. And there is more. The CD is a
    searchable database that can be used as an identification tool
    supplementary to the keys. Possible inputs are measurements, colour
    and country of origin. Or the user can scroll between closely related
    species and compare high-resolution colour images of the lateral views
    of major and minor workers and frontal views of heads.

    Why is this book so heavy? Why are there so many species of Pheidole?
    Wilson devotes an introductory chapter to discussing the origins of
    hyperdiversity. It is an important essay. If the numbers of species
    within, say, the genera of a family are rank-ordered as a histogram,
    its shape will be a hollow curve and this signature is a
    characteristic of the living world as a whole. A large number of
    genera contain a single species while only very few contain large
    numbers of species.

    Hyperdiversity is a rare extreme of one end of the hollow curve. A
    succession of scientists (for more than eighty years) have tried to
    pin down both the how -the precise mathematical form of the curve, and
    the why - the underlying model or evolutionary mechanism that
    generates this elegant mathematical generality among groups of
    organisms. The hollow curve approximates to a logarithmic series and
    belongs among the family of curves that derive from the negative
    binomial; but the model that generates this curve is obscure. However,
    empirical models that assume sequential origin of groups through time
    and a cyclical peaking and subsidence of diversity can, says Wilson,
    approximate the observed distribution.

    Factors that have been demonstrated to contribute to high species
    diversity are "small size, right demographic factors, preemption
    during colonization and subsequent incumbency, and a suite of key
    adaptations potent in opening new niches or excluding competitors". So
    nothing new there then. Small organisms are suggested to be more
    adaptable to change and the pressure of environmental stress, while
    large organisms do better in stable environments. Oscillation between
    environmental stability and instability will cull the size extremes.
    The diversity of organisms in the small-to-medium-size classes is
    boosted by higher speciation rates and a better fit to the fine
    fractal topography of environments. The most diverse groups have other
    common features too - short generation times and a brief average
    lifespan, superior dispersal ability and high resource availability.
    Sewall Wright's 1931 theory still holds, that species that are divided
    into demes (demonstrably discrete populations) speciate more rapidly
    than species with amorphous populations. But speciation may be offset
    by extinction. And the Pheidole story is complicated by these being
    atypical organisms - they are social.

    Two competing hypotheses may apply here: one says that social
    organization is primitive but successful and drives diversity, the
    other that sociality preadapts organisms to coping with new
    environmental challenges, aka speciation opportunities. Speculation is
    rife and there is little here to hang one's hat upon. Wilson returns
    to his original thesis of pre-emption and incumbency. The former
    involves possibly two key factors - dispersal ability and
    breakthrough; the latter is the ability to create and use new niches
    or to elbow one's way into and take over existing niches.

    Incumbency is simply holding the fort - possession is nine-tenths of
    the evolutionary game. Wilson likens pre-emption and incumbency to
    industrial development. And in terms of growth, success in both
    industry and the natural world breeds success. Whether the analogy
    extends to long-term sustainable diversity is another matter. In the
    end, Wilson admits that the "hypotheses, correlative analyses and
    speculations . . . have been very broad, even abstract . . .". He
    focuses on the big question "What are the adaptations that promote
    ecological dominance within a clade (the complete group of taxa
    derived from a single common ancestor)?". It is a deceptively simple
    question but one that is fiendishly difficult to answer, or even to
    plan how to answer. And answering that cannot of itself take us to
    conquer the Santa Rosalia question of why there are so many species of
    Pheidole. What is so special about Pheidole?

    The hypothesis that Wilson eventually tenders is that the breakthrough
    novelty in Pheidole is the existence of the large-headed major-worker
    caste with reduced sting and increased abilities in defensive
    secretions produced by exocrine glands.

    As a group, Pheidole places extreme reliance on these majors for
    colony defence and they form "a highly mobile strike force" while the
    minor workers are the drudges. The minors "have the appearance of a
    'throwaway' caste, that is, small, light, cheaply manufactured and
    short-lived". Pheidole is "an unusually resilient superorganism able
    to expend and replace minor workers readily while utilizing the major
    subcaste both for defense and as an emergency labor force in the event
    of severe depletion of the minors". We are left admiring the elegance
    of his summation but still very conscious that the precise "why" of
    hyperdiversity has not been satisfactorily answered.

    There are moments in history when one wishes one could have been a fly
    on the wall or, in this case, a fly on the windshield. In the summer
    of 1952, Wilson was a graduate student at Harvard and joined forces
    with another student, Tom Eisner, to "undertake a major exploratory
    venture". With a $200 grant and an old Chevrolet, they travelled
    12,000 miles through forty-eight states to "get acquainted with the
    American landscape and its insects". It was both an entomological and
    an intellectual odyssey, and the two became and remain great friends
    as well as two of the most influential and powerful forces in
    entomology. Wilson's generous foreword to Thomas Eisner's For Love of
    Insects sets the stage for a remarkable memoir by a remarkable man.

    Opening with Martin Rees's opinion that "what makes things baffling is
    their degree of complexity, not their sheer size . . . . a star is
    simpler than an insect", Eisner's raison d'etre for his science is
    deceptively simple. "Insects survive because they have special
    strategies for doing so . . . . How it is that one goes about
    deciphering these strategies, and how serendipity, group effort and
    sheer good luck combine to provide momentum in such research, are what
    I have attempted to convey . . .". Eisner is a chemical ecologist, and
    his career has been spent unravelling some of the most bizarre stories
    of how insects use a combination of chemicals, sometimes simple and
    sometimes complex, and sophisticated morphological structures to
    defend themselves, their colonies, their mates and even their
    offspring. And it is not just the use of chemicals in defence -
    insects communicate using scent or pheromones, sound, and visual
    signals, or a combination of these.

    When defensive chemistry is involved also in reproduction and the
    protection of offspring the story can become quite extraordinary, and
    the investigation of the extraordinary calls for extraordinary
    methods. Eisner's book compels and fascinates at a variety of levels.
    It probes the ways in which insects use chemicals, and documents the
    ways in which an investigator poses the questions and teases out the
    answers. Eisner has covered an immense territory in his career - he
    has been an unashamed opportunist, observing a phenomenon that others
    may have taken for granted, asking why and how and being richly
    rewarded for his curiosity. He tells his stories in the most
    accessible way. His experiments are simple - he approaches problems
    using a logical technique he calls "biorationality" - the formulation
    of a sequence of linked questions which, if answered, explain the
    function and adaptive significance of a structure or behaviour,
    compare parallels or homologies in other organisms, and explain the
    origin or evolution of the feature. The sheer elegance of his approach
    is spellbinding. And the photographs that document his explorations
    are remarkable - every experimental tale here is beautifully
    illustrated. A single example from the many will give a little of the
    flavour of his stories.

    Utetheisa moths have a wingspan of a little more than an inch, and are
    speckled black, white and bright rose; the English vernacular name of
    the African species that is an occasional migrant to British shores is
    the Crimson Speckled. They are diurnal, and that behaviour, combined
    with their bright coloration, makes them prime suspects to be
    distasteful to predators. In 1966, Eisner observed a Utetheisa
    ornatrix, the Florida species, fly into a spider's web. Instead of
    struggling, the moth froze and waited. The spider inspected it and
    then cut it free. "Being witness to that act of rejection . . . was a
    compelling experience", says Eisner.

    Spiders consistently rejected Utetheisa. Eisner noticed that when
    disturbed, the moths emitted a foam from the back of the neck. The
    foam proved to be haemolymph, insect "blood", mixed with air. But
    spiders rejected moths whether or not they foamed. Tests with
    separated wings and bodies showed that all parts of Utetheisa were
    rejected by spiders. The foam seemed to be an added deterrent,
    suggesting Utetheisa was thoroughly nasty on the inside as well as the
    outside.

    Utetheisa ornatrix caterpillars feed on Crotalaria, the rattlepod.
    This wild bean is toxic and has an unpleasant reputation as a cattle
    poison, for its seeds and leaves contain pyrrolizidine alkaloids
    (PAs).

    Other species of Utetheisa feed on plants of the borage family which
    are known also to contain PAs. Could adult Utetheisa carry poisons
    sequestered during larval feeding, as does the Monarch butterfly?
    Eisner's lifelong collaborator, Jerry Meinwald, and his research group
    took up the challenge and showed that the moths indeed harboured a
    high concentration of PAs. But did PAs confer protection from
    predators? Eisner's group were able to rear Utetheisa on an artificial
    diet made either from pinto beans (PA-free) or Crotalaria beans
    (PA-rich). Adults reared on pinto beans did not contain PAs and were
    eaten by spiders. Adults reared on the Crotalaria diet were armed with
    PAs and rejected by spiders. The final test was to taint mealworms
    (usually eaten with gusto by spiders) with PAs and offer them to
    spiders; they were rejected. Female Utetheisa passed PAs into their
    eggs and these protected the eggs from predation by Leptothorax ants.
    Eggs laid by PA-free females were not protected. Ants actually
    developed a long-term aversion to PA-tainted eggs, and were able to
    remember the experience and avoid Utetheisa eggs for at least a month
    after being exposed. Larvae of lacewings were also able to
    discriminate between eggs with and without PAs - they sampled eggs by
    piercing them and sucking out the contents with their hollow jaws.
    PA-laden batches, each of ten eggs, were avoided after sampling of
    just two or three eggs.

    Caterpillars deficient in protective PAs were clearly "aware" of this
    deficiency and would attack and eat eggs and larvae of their own
    species that contained PAs. Clearly PAs played an enormous part in the
    life of Utetheisa.

    Eisner's team began to tease apart the secrets of courtship, mating
    and reproduction. They found that, unsurprisingly, Utetheisa females
    "called" males using an airborne pheromone, as do most Lepidoptera
    species. But what was remarkably different was that the pheromone was
    emitted in precisely timed pulses and they were able to show how the
    glands operated to achieve this. The reason for pulsing is still
    unclear, but it seems to save on chemical resources as well as provide
    a way of refining the male's search strategy at close range.

    At this point the lazy researcher might have just assumed "female
    attracts male and Bob's your uncle". Eisner instead became interested
    "in the behavior that comes into play once the male encounters the
    female . . . . Utetheisa, before mating, engages in 'pillow talk'. We
    decided that it might be worth listening in .

    . .". Videotape of mating encounters showed how the male flew upwind
    to the female, hovering beside her and making contact with antennae
    and legs; the male then abruptly flexed his abdomen, thrusting the tip
    towards the female; she raised her wings, exposing her abdomen, and
    the male landed beside her, made genital contact and copulated. The
    abdominal action lasted barely a third of a second.

    More refined high-speed photography and some careful dissection showed
    that two balloon-like structures set with specialized scales that
    formed brushes in the male abdominal tip were extruded and presented
    to the female in that one-third of a second. These brushes had been
    shown to be pheromone-carriers in other moth species and Jerry
    Meinwald's team quickly showed that the coremata (the correct term for
    the brushes) were loaded with hydroxydanaidal (HD), a derivative of
    PAs.

    Moths that were PA-free did not carry HD. Male moths with no HD, or
    which had had their coremata surgically removed, were frequently
    rejected by females.

    What was the message carried to the female in the HD? Eisner's team
    showed that the HD concentration in the coremata of the adult male was
    proportional to the quantity of PAs it had ingested and stored as a
    larva. And then it became clear.

    They found that eggs laid by a PA-free female could contain PAs and be
    protected against predation; all the female had to do was to mate with
    a PA-loaded male (PA-free males and females produced PA-free eggs).

    Males transmit protection to their offspring by giving the female a
    gift of PA during copulation (as a component within the liquid of the
    spermatophore, the sperm "packet"); about one-third of the egg's PA is
    derived from the father. The male's wafting of his HD-loaded scent
    brushes in front of the female proclaims his PA loading quantitatively
    - he offers a nuptial gift with, as it were, the value marked on the
    box. His gift, added to her PA loading (for in nature all females have
    at least a trace of PA), protects their eggs and also protects her
    while she lays them - she mobilizes his PA gift immediately; a PA-free
    female becomes distasteful to spiders within five minutes of
    insemination.

    Mating provides female Utetheisa not just with PAs but also with
    nutrients, notably proteins, and minerals in the spermatophore.
    Females mate more than once, and one final twist in the extraordinary
    story of this moth is that the female can choose which spermatophore
    to use to fertilize her eggs; she chooses the largest.

    And spermatophore size is correlated positively with the physical size
    of the male and his level of PA loading. Eisner's team were able to
    demonstrate that body mass is a heritable feature, and thus close the
    circle. The female selects a mate that will give her larger sons with
    potentially increased fitness and larger daughters with greater
    fecundity. And she makes that choice using the male's pheromone his HD
    level - as a chemical yardstick. She does not or cannot discriminate
    between males of different sizes or with different PA concentrations.
    She bases her genetic future on a one-third-of-a-second flash of the
    male's coremata.

    The dustjacket portrait of Thomas Eisner sums up this book. He is
    riding a bicycle backwards, no hands. As the author, so the subjects:
    who dares, wins.