The Parasitic Wasp's Secret Weapon

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The Parasitic Wasp's Secret Weapon
The Parasitic Wasp’s
                        Secret Weapon
                  Parasitic wasps must develop inside living caterpillars.
                    They survive this hostile environment by smuggling
                   in a virus that suppresses their host’s immune system

                                                      by Nancy E. Beckage

T          his caterpillar will never be-
           come a moth. It lurks deep in
           the foliage of a tasty tomato
plant, hidden from predators, but its
enemy has found it anyway. In search
                                              will die as well. Yet the caterpillar can-
                                              not be allowed to gain the upper hand
                                              using its immune defenses. Much of the
                                              responsibility for maintaining this deli-
                                              cate balance falls to the wasp’s viral ac-
of a nanny for her offspring, the para-       complice. Like the wasp, many parasites
sitic wasp has homed in on the distinc-       of insect hosts have evolved associa-
tive scent of her lepidopteran victim         tions with bacteria and viruses that help
and its lunch. Now the tiny wasp in-          them perform their often deadly deeds.
jects a clutch of eggs through the cater-                                                  the University of
pillar’s tough cuticle and into its body                Microbial Weapons                  Cambridge sus-
cavity, where her larvae will thrive by                                                    pected that female
feeding on their living nursery. At a crit-
ical moment in development, the wasp
larvae will burst through the flanks of
                                              A    simple example of such a partner-
                                                     ship occurs in certain parasitic
                                              worms that carry a virulent bacterium
                                                                                           Venturia wasps in-
                                                                                           ject substances re-
                                                                                           quired for successful
the caterpillar to spin their cocoons on      in their digestive tracts. These worms       development of their
its surface. These wasps eventually de-       regurgitate the bacteria into their insect   progeny into host larvae
part as adults, metamorphosis com-            hosts, killing the hosts within days of      along with eggs during
plete, but their host is now destined to      infection. The rapidly dividing bacteria     the process called oviposi-
die as a caterpillar.                         are an immediate food source for the         tion. In particular, Salt noted
   If this were a one-on-one interspecies     developing worms, and they provide           that the ovary of the female
scuffle, the caterpillar might stand a        further sustenance by secreting diges-       wasp harbors substances that
chance—it has an immune system capa-          tive enzymes that soon turn the host ca-     prevent destruction of wasp eggs
ble of engulfing and killing invading         daver into a nutrient-rich soup. In re-      by the caterpillar’s immune cells.
wasp eggs before they can do permanent        turn, the bacteria benefit by using the         Normally, injected wasp eggs float
harm. The wasp, however, does not             worms as vehicles for invasion of new        freely in the bloodlike fluid, called the
come to this encounter alone. In addi-        hosts. These interacting partners are        hemolymph, that fills the body cavity of
tion to her eggs, she injects hordes of       strictly independent organisms—they          the caterpillar. When Salt washed the
virus particles. These viral warriors ra-     do not share genes.                          wasp eggs prior to injection, however,
pidly defeat the caterpillar’s immune re-        In contrast, the interaction between      they provoked a rapid immune response.
sponse, tipping the balance of power in       endoparasitic wasps and the virus they       These eggs, stripped of an unidentified
favor of the wasp progeny. The cater-         exploit is more intimate. Not only are       factor, were quickly attacked by the
pillar, doubly parasitized, slowly ceases     the fates of the partners intertwined, but   host’s immune cells and ultimately killed.
feeding, fails to pupate and dies a pre-      their genetic material is also permanent-    In 1973 electron micrographs taken by
mature death.                                 ly mingled. And the relationship goes
   Host-parasite relationships such as        further—the wasp and the virus possess
those involving the wasp, the virus and       related genes. All this raises a thought-
                                                                                           WASP AND CATERPILLAR are the Da-
the doomed caterpillar are among the          provoking question: Are the wasp and         vid and Goliath of the insect world. The
most complex in nature. The wasp is an        the virus two entities or one?               huge caterpillar’s immune system threat-
endoparasite—it must develop inside its          The first hint that endoparasitic wasps   ens the wasp’s eggs, which must mature
host. If the caterpillar dies before the      might have unusual weapons in their          inside a living host. But the tiny wasp pre-
wasp larvae are properly fed, the wasps       arsenal came in 1965. George Salt of         vails using a deadly weapon: a virus.

82    Scientific American November 1997 Copyright 1997 Scientific American, Inc.                  The Parasitic Wasp’s Secret Weapon
The Parasitic Wasp's Secret Weapon
ROBERTO OSTI

Copyright 1997 Scientific American, Inc.
The Parasitic Wasp's Secret Weapon
WASP LAYS                                                                         WASP LARVAE PREVAIL
                                                                                                      EGGS IN
                                                                                                    CATERPILLAR
LAUREL ROGERS; STEVEN H. HARWOOD (top and bottom micrographs); MARK D. LAVINE (center micrograph)

                                                                                                                                   EGG IS ACCOMPANIED BY
                                                                                                    a                             OVARIAN FLUID AND VIRUS

                                                                                                                            EGGS ARE                                 CATERPILLAR’S IMMUNE SYSTEM
                                                                                                                            WASHED                                       FIGHTS OFF INVASION

                                                                                                                                    EGGS WITHOUT
                                                                                                                                    OVARIAN FLUID (AND VIRUS)
                                                                                                    b                               ARE INJECTED INTO CATERPILLAR

                                                                                                                                                                                      WASP LARVAE PREVAIL

                                                                                                                                                             WASHED EGGS
                                                                                                                                                           ARE INJECTED INTO
                                                                                                    c                                                    CATERPILLAR WITH VIRUS

                                                                                                        BATTLE OF THE INSECTS rages between the caterpillar and              not so fortunate. In the laboratory, however, wasp eggs that have
                                                                                                        the wasp. Wasp eggs escape attack by the caterpillar’s immune        been washed lack the protective virus (b) and are rapidly en-
                                                                                                        system thanks to a virus injected into the caterpillar by the wasp   gulfed by the caterpillar’s immune cells (center micrograph); no
                                                                                                        along with her eggs (a). The virus disables the caterpillar’s im-    wasps survive this encounter. Injecting pure virus along with the
                                                                                                        mune cells, allowing the free-floating eggs (top micrograph) to      washed eggs (c) allows the wasp eggs (bottom micrograph) to
                                                                                                        develop into normal wasp larvae. The fate of the caterpillar is      develop into larvae and emerge from the caterpillar.

                                                                                                        Susan Rotheram, also at Cambridge,            purified virus. But how exactly do the       wasps: certain cells, known as hemo-
                                                                                                        offered a clue to the identity of the pro-    viruses—today called polydnaviruses          cytes, circulating in the caterpillar’s blood
                                                                                                        tective substance. These images showed        (pronounced “puh-LID-nah-viruses”)—          undergo rapid physical transformation.
                                                                                                        that the surface of a Venturia egg be-        disable the caterpillar immune system?       Graduate student Mark D. Lavine has
                                                                                                        comes impregnated with viruslike parti-                                                    seen these effects within a few hours of
                                                                                                        cles as it passes through the wasp’s ovi-                Immune Deficiency                 oviposition. Affected hemocytes “round
                                                                                                        duct during oviposition.                                                                   up,” failing to adhere to substrates such
                                                                                                           Nearly a decade later Donald B.
                                                                                                        Stoltz of Dalhousie University conduct-
                                                                                                        ed an extensive taxonomic survey of
                                                                                                                                                      T    o answer this question, my col-
                                                                                                                                                           leagues and I study the parasitic
                                                                                                                                                      wasp Cotesia congregata, which can
                                                                                                                                                                                                   as glass or parasite eggs. They also un-
                                                                                                                                                                                                   dergo extensive blebbing, or pinching
                                                                                                                                                                                                   off of bits of their membrane and cell
                                                                                                        parasitic wasps in collaboration with         lay hundreds of eggs in each caterpillar.    contents. The damaged hemocytes
                                                                                                        S. Bradleigh Vinson of Texas A&M              These eggs hatch into larvae that dine       clump together and are removed from
                                                                                                        University. They showed that viruslike        on the host’s hemolymph fluid instead        circulation. Overall, this transforma-
                                                                                                        particles are invariably found in certain     of consuming its tissue, thereby allow-      tion bears a striking resemblance to the
                                                                                                        wasp species that develop as internal         ing the infected caterpillar to survive      cell suicide, or apoptosis, that occurs in
                                                                                                        parasites of lepidopteran hosts. More-        well past emergence of the wasp proge-       mammalian cells [see “Cell Suicide in
                                                                                                        over, they observed that these viruses        ny. Manduca sexta, the tobacco horn-         Health and Disease,” by Richard C.
                                                                                                        replicate exclusively in the ovarian tis-     worm, serves as our model host. Any-         Duke, David M. Ojcius and John Ding-
                                                                                                        sue of female wasps. During oviposi-          one who grows tomatoes has probably          E Young; Scientific American, De-
                                                                                                        tion, the wasp injects thousands of viri-     had a run-in with these giant leaf-green     cember 1996].
                                                                                                        ons into the caterpillar along with one       caterpillars, which forage on tomato,           Granulocytes and plasmatocytes are
                                                                                                        or more eggs.                                 tobacco and jimsonweed and often             among the caterpillar hemocytes most
                                                                                                           It seemed reasonable to suspect that       grow to the size of a man’s little finger.   affected by parasitism; Michael R.
                                                                                                        these viruses are the ovary-derived sub-      Tobacco hornworms are convenient to          Strand of the University of Wisconsin
                                                                                                        stances that accompany wasp eggs into         work with in the laboratory: obtaining       has shown that granulocytes in particu-
                                                                                                        the host and squelch the host’s immune        blood samples from these enormous cat-       lar die by apoptosis. These are exactly
                                                                                                        response. The evidence was purely cir-        erpillars is easier than obtaining samples   the host immune cells that respond to
                                                                                                        cumstantial until 1981, when Stolz, Vin-      from mice.                                   foreign objects, including Cotesia eggs.
                                                                                                        son and their co-workers finally con-           We have observed one immediate con-        In a normal immune response, granulo-
                                                                                                        firmed that this job can be performed by      sequence of the parasitism by Cotesia        cytes first release granules that coat the

                                                                                                        84    Scientific American November 1997 Copyright 1997 Scientific American, Inc.                  The Parasitic Wasp’s Secret Weapon
invading egg. Plasmatocytes then ad-         protein inside hemocytes one day after         hemocytes. Webb has shown that imme-
here to the egg surface in multiple lay-     oviposition, when these cells were quite       diate but short-term protection against
ers, forming a thick capsule that even-      disabled. We continued to find evidence        immune cells is conferred by ovarian
tually kills the egg inside. Selective re-   of EP1 in the caterpillar for six days;        protein molecules injected directly into
moval of the granulocytes and the            hemocyte function returned to normal           the host by the wasp. The job of long-
plasmatocytes from circulation disables      on the eighth day—but too late for the         term protection then falls to the polyd-
the caterpillar’s first line of defense      caterpillar to kill the wasp larvae.           navirus through sustained viral protein
against the endoparasite. Similar phe-          Researchers led by Otto Schmidt of          production in caterpillar cells.
nomena occur during human immuno-            the University of Adelaide have found a
deficiency virus (HIV) infection in hu-      similar correlation in a different host-                Arresting Development
mans. In that case, the virus targets        parasite pair: hemocytes first become
lymphocytes, causing the clumping and
apoptotic death of the cells. Opportu-
nistic infectious agents are then free to
                                             damaged during the brief period when
                                             viral protein is produced—then immune
                                             response rallies in two or three days. We
                                                                                            A    nother important aspect of the Co-
                                                                                                  tesia-Manduca-polydnavirus tri-
                                                                                            partite relationship (and the one that
ravage the victim, much like the wasp        speculate that hemocyte damage occurs          first piqued my interest in the field) is
progeny that overtake their unfortunate      as long as such viral proteins persist;        the way the parasite manipulates the
caterpillar host.                            once viral protein levels drop, damaged        development of the host. A growing in-
   When we inject unparasitized tobacco      hemocytes would recover or be replaced,        ternal parasite benefits by extending the
hornworm larvae with purified polyd-         replenishing the functional supply.            interval over which its host remains a
navirus, caterpillar hemocytes undergo          One consequence of this timing is           feeding larva. For this reason, many en-
changes in appearance and behavior           that the host immune response resumes          doparasites develop strategies to delay
analogous to those we observe in nor-        in full force before developing wasps are      host metamorphosis. I was particularly
mal parasitism. But if we chemically in-     ready to leave the caterpillar. Unlike vul-    interested by the case of the tobacco
activate the virus prior to injection, the   nerable eggs or young larvae, however,         hornworm parasitized by Cotesia, be-
hemocytes remain unaltered. This re-         older wasp larvae seem able to with-           cause this host remains developmental-
sult suggests that virus capable of di-      stand active immune cells on their own.        ly stunted long after the wasp progeny
recting manufacture of viral proteins is     Polydnavirus provides a long but tem-          leave the body cavity; the caterpillars
required for immune suppression.             porary reprieve from immune attack,            often linger two weeks before dying.
   Graduate student Steven H. Harwood        allowing the wasps to become mature               Developmental arrest in lepidopteran
has shown that polydnaviral proteins         enough to protect themselves.                  hosts is mediated through the endocrine
do indeed appear rapidly in the cater-          Bruce A. Webb of the University of          system. I studied endocrine disruption
pillar host. We detect the first evidence    Kentucky, who works with parasitized           caused by parasitism as a graduate stu-
that polydnaviral genes are active with-     tobacco budworms, has discovered how           dent in Lynn M. Riddiford’s laboratory
in 30 minutes of oviposition. By this        the wasps fill one final chink in their        at the University of Washington. There
time viral particles have spread through-    immune suppression armor. Although             I observed that the concentration of a
out the host, entering cells, including      the cellular immune response by the            key hormone regulating metamorpho-
hemocytes. In our tobacco hornworm           caterpillar is essentially immediate, there    sis is disturbed after parasitism of to-
system, we have also shown that at least     is a lag before polydnaviral proteins are      bacco hornworms by C. congregata.
one polydnavirus-encoded protein is          available to alter the behavior of host        The level of juvenile hormone (JH) is
produced inside host hemocytes follow-
ing parasitism. This protein is called
EP1, for “early protein 1.”
   We took great care to establish that
                                                             Enlisting Insects in the War on Weeds
EP1 is in fact a polydnaviral protein.
EP1 production can be induced in to-
bacco hornworm larvae by injection of
                                             W          asps and viruses are not the only organisms capable of hardball tactics: hu-
                                                        mans are past masters. And lately scientists have turned caterpillars and their
                                             parasites into lethal weapons against weeds. Their worthy opponent is kudzu, a fast-
polydnavirus alone, suggesting that the      growing, pernicious climber that carpets seven million acres in the southern U.S.
EP1 gene resides in the genome (the             Entomologist David Orr and his colleagues at North Carolina State University have re-
characteristic set of genes) of the virus;   cently deployed soybean looper caterpillars to combat kudzu. In field tests the loopers
alternatively it could reside in the ge-     defoliate the weed, and Orr believes the plants’ efforts to replace lost leaves will slowly
nome of the host and merely be activat-      exhaust their enormous root systems (a single plant can have roots that weigh as much
ed by the virus. We deduced part of the      as 300 pounds).
sequence of the gene encoding the EP1           Because soybean loopers eat crops as well as kudzu, each caterpillar enters the field
protein and then searched for this se-       equipped with a safety mechanism to prevent its escape—parasitic wasps that execute
quence in various organisms. We turned       the caterpillar as it spins its cocoon, ensuring that no moths will emerge to fly away and
up no such gene in Manduca but in-           reproduce. An added benefit is that the parasitized loopers eat more kudzu: the wasps
stead found the EP1 gene in the polyd-       extend both the feeding interval of the caterpillars and their appetite.
navirus genome. Intriguingly, manufac-          It is not clear how the eggs of this wasp, Copidosoma truncatellum, escape attack by
ture of this polydnaviral-encoded pro-       the immune system of the caterpillar; the wasp does not carry polydnaviruses. Several
tein correlates temporally with the most     wasps that do carry polydnavirus have also been used in biological-control strategies,
dramatic effects of parasitism on host       though, often as weapons against populations of pest insects, including destructive
hemocytes.                                   fruit flies, moths and aphids.                                       —Mia Schmiedeskamp
   We detected high levels of the EP1

The Parasitic Wasp’s Secret Weapon             Copyright 1997 Scientific American, Inc. Scientific American November 1997            85
dramatically elevated in parasitized         wasp chromosomes. No virus-free indi-
hosts, never descending to the low level     viduals have ever been identified in
needed for pupation. The high levels of      wasp species that carry polydna-
JH are probably caused by a lack of          viruses. Virus and wasp ap-
sufficient juvenile hormone esterase, an     pear to be permanent and
enzyme that clears JH from the organ-        integral partners.                     N
                                                                                HO ORM
ism. Parasitism apparently leads to sus-        Unlike typical infec-               R
                                                                                LIF NWO AL
tained low esterase levels, in a manner      tious viruses that usurp              EC
                                                                                      YC RM
                                                                                        LE
that prevents pupation even after de-        the replication ma-
parture of the wasps.                        chinery of their
   It turns out that developmental arrest    hosts to repro-
is largely executed by polydnavirus, al-     duce wildly,
though the presence of the wasp itself is    polydnavirus
needed to obtain full arrest. When we in-    reproductive
ject unparasitized larvae with low doses     success is af-
of polydnavirus, they fail to pupate         fected by the
normally. The amount of virus required       survival of each
to retard development appears to be less     and every wasp. For
than that required to suppress the im-       every wasp that is pro-
mune response. In fact, postdoctoral         duced, a chromosomal
fellow Mitch Dushay showed that eggs         copy of the virus is pro-
that have been washed prior to injec-        duced. This intimate associa-
tion retain trace amounts of virus parti-    tion of the genetic material of
cles or viral proteins that do not suffice   wasp and virus explains the seeming-
to prevent encapsulation by immune           ly selfless role of the virus in supporting
cells but may cause developmental fail-      wasp parasitism. The success of polyd-
ure of the host. Polydnavirus may also       navirus depends on efficient reproduc-           quired the ability to copy and package
contribute to developmental effects          tion of the wasp, which in turn depends          a subset of useful genes selectively from
even after departure of the wasps from       on an essential host-parasite relation-          their own genomes, for shipment into
the host. We speculate that the virus re-    ship. Any role the virus plays in ensur-         caterpillar cells. Work by Webb and
mains as a latent infection in the cater-    ing the success of the parasite also en-         Summers on wasp venom proteins may
pillar—perhaps mediating lasting effects     sures the success of viral transfer to the       fit with this last hypothesis.
on development.                              next generation.                                    These researchers have found that
   Polydnavirus is clearly responsible          Because viral transmission from wasp          some wasp venom genes are similar to
for manipulating a number of develop-        to wasp takes place through inheritance          polydnaviral genes. Moreover, antiven-
mental and immune programs of the            of a virus integrated into the chromo-           om antibodies raised in the laboratory
caterpillar host in a manner that is         some, there must be some other ratio-            also recognize viral proteins that are im-
beneficial to the wasp. In many ways,        nale for the mass production of virus in         portant for manipulation of the cater-
the virus is essential to successful para-   the wasp’s ovaries. In fact, the packaged        pillar. It seems, then, that wasp venom
sitism. The amazing strength of this re-     viruses produced at this step seem to be         genes and polydnaviral genes may be
lationship between wasp and polyd-           useless for the typical viral mission of         evolutionarily related. This result is es-
navirus becomes even clearer when one        infection with intent to replicate—but           pecially exciting because certain wasp
considers the genetics of the partners.      they are masters of host manipulation.           venom proteins are known to play a
                                             Viruses are expert at spreading through-         supporting role in manipulating cater-
          Permanent Partners                 out a host and entering host cells. Para-        pillar physiology.
                                             sitic wasps appear to have harnessed                In one evolutionary scenario, initially

T    he size and complexity of polydna-
     viral genomes greatly exceeds that
of other DNA viruses: each polydna-
                                             this talent to target useful viral protein
                                             production to caterpillar cells, allowing
                                             for insider manipulation of their host’s
                                                                                              independent polydnaviruses may have
                                                                                              picked up useful venom genes from the
                                                                                              wasp genome. In another scheme, the
virus comprises up to 28 separate circles    biology.                                         wasp may have found an incredibly ef-
of double-stranded DNA (thus their              The integration of polydnaviruses             ficient way to utilize its own venom
name, from “polydisperse DNA virus-          into wasp chromosomes prompts ques-              proteins, by copying their genes, pack-
es”). In 1986 Jo-Ann G. W. Fleming and       tions about the origin of the virus. A           aging them and routing them to cater-
Max D. Summers of Texas A&M dis-             typical answer might be that the viruses         pillar cells where they can maintain a
covered that the extremely complex           originated as independent pathogens of           sustained effect. Either scenario results
polydnavirus genome is integrated into       the caterpillar hosts, or of the wasps           in increased fitness of both the wasp
the genome of both male and female           themselves, and later combined with              and virus; either way the genetic bound-
wasps. This viral DNA is thought to be       the wasp DNA. A much more intrigu-               aries between the wasp and virus are
scattered throughout the wasp chromo-        ing possibility is suggested by the ap-          obscured.
somes. Wasp inheritance of the virus         parently permanent and exclusive asso-              Whatever the origins of the polyd-
appears to be strictly Mendelian—the         ciation of viral DNA with wasp DNA.              naviruses, their associations with wasps
viral sequences are copied and passed        Perhaps there was never a separate viral         and caterpillars offer rich opportunities
to successive generations as part of the     entity. Instead wasps may have ac-               for the study of evolutionary biology.

86   Scientific American November 1997 Copyright 1997 Scientific American, Inc.                      The Parasitic Wasp’s Secret Weapon
WASP INJECTS EGGS
AND POLYDNAVIRUS                                                                                       WASP LARVAE EMERGE
 INTO CATERPILLAR                                                                                       FROM CATERPILLAR
                                                                                LARVA

                                             WASP
                                             EGG

                                                                       VIRUS ENTERS
                                                                     CATERPILLAR CELLS
   HO IFE C
   AL NW CLE
     TE OR

                                                 L
     L
      R Y

                                             VIRA AY                                VIRUS REPLICATES
       RE M

                                               H W
          D

                                            PAT                                         IN WASP
                                                                                     OVARIAN CELLS
                                     P
                                WAS LE
                                 E CY C
                              LIF
                                                  VIRUS READY
                                                    FOR INJECTION
                                                     INTO NEW HOST

                                                                                                       PUPA

    INTERTWINING LIFE
    CYCLES reveal the relations
    among caterpillar, wasp and
    polydnavirus. The normal horn-
    worm life cycle (left) is disrupted
    when a wasp injects her eggs and polyd-
    navirus. The wasps mature and reproduce
    normally (blue circle), but the hornworm dies prema-
    turely (yellow circle, right). This sabotage is orchestrated
    by polydnavirus, which enters and disables caterpillar
    cells (brown circle). Wasps inherit the virus in their chro-

                                                                                                                                                  ROBERTO OSTI
    mosomes, and the virus multiplies in the developing
    wasp’s ovaries in preparation for the next round of battle.
                                                                                  CATERPILLAR DIES

    The vicious tactics of the wasp and its         Scientific American, April 1993].                between wasp and virus is so intimate
    viral accomplice against their hijacked           Endoparasitic wasps invariably kill            that it blurs interspecies genetic bound-
    caterpillar host argue against the tenu-        their hosts. The event is exquisitely            aries. The complex question of why the
    ous hypothesis that the most highly             timed and coordinated, however, to en-           caterpillar does not become a moth
    evolved parasites exhibit only minimal          sure the success of the wasp. In beauti-         should keep a raft of scientists from
    virulence to their hosts [see “The Evo-         ful contrast to these hardball tactics,          evolutionary biologists to endocrinolo-
    lution of Virulence,” by Paul W. Ewald;         the mutually advantageous relationship           gists busy for years to come.           SA

                              The Author                                                          Further Reading
       NANCY E. BECKAGE is associate professor of entomology at           Polydnaviruses: Mutualists and Pathogens. Jo-Ann G. W. Flem-
    the University of California, Riverside, where she has been on the     ing in Annual Review of Entomology, Vol. 37, pages 401–426; 1992.
    faculty since 1990. Her interests include the strategies adopted by   How Parasitic Wasps Find Their Hosts. James H. Tumlinson, W.
    parasites and pathogens to disrupt development of host species         Joe Lewis and Louise E. M. Vet in Scientific American, Vol. 268, No.
    and the coevolutionary relationships of host organisms with para-      3, pages 100–106; March 1993.
    sites. Previously, Beckage held positions in the U.S. Department of   Polydnaviruses: Potent Mediators of Host Insect Immune
    Agriculture Stored Products Insects Research Unit at the Universi-     Dysfunction. M. D. Lavine and N. E. Beckage in Parasitology To-
    ty of Wisconsin and at the Seattle Biomedical Research Institute.      day, Vol. 11, No. 10, pages 368–378; 1995.
    She received a Ph.D. from the University of Washington in 1980.       Parasitic Wasps. Donald L. J. Quicke. Chapman & Hall, 1997.

    The Parasitic Wasp’s Secret Weapon                 Copyright 1997 Scientific American, Inc. Scientific American November 1997           87
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