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Describe the main idea, or argument, of each piece. What did the two readings have in common? What was distinct about each? In what way did the form and style of the writing affect the idea being presented? Your thoughts? At least 3 paragraphs.
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We Are A Teeming
Wilderness
by Shena McAuliffe
I can tell you the exact date that I began to think of myself in the first-person plural — as a
superorganism, that is, rather than a plain old individual human being…[These several hundred
microbial species with whom I share this body] which number around 100 trillion, are living (and
dying) right now on the surface of my skin, on my tongue and deep in the coils of my intestines.
-Michael Pollan, “Some of My Best Friends are Germs”
Do I contradict myself?
Very well then I contradict myself,
(I am large, I contain multitudes.)
-Walt Whitman, “Song of Myself”
We, the superorganism known as “Glenn,” often envision an infographic of ourself in the shape
of a man. This infographic is a veritable stained glass window of colors and shapes. We imagine
our mouth shape as red, esophagus yellow, sinuses green, gut purple, and stomach orange. Our
brain is a quiet gray, unless pulled out for close focus in an infographic of its own. Our groin is a
fecund garden. Under a microscope, our groin would appear as a jungle, full of tiny monkeys
climbing on wiry trees. The groundcover absolutely crawling with life. Blooming and dying and
blooming.
Sometimes we, Glenn, swap cells with other superorganisms. We’ve exchanged plenty of gypsy
microbes with the superorganism that goes by “Sophie Izbal.” Sophie is a garden, too, of course,
a verdant Eden. Her infographic would be more purple than ours—female superorganisms
have longer intestines—and her jungle includes a tropical cavern. With Sophie, we crossfertilize. We diversify our ecosystem. Some of us who are now Glenn used to live in or on
Sophie. We traveled in caravans from pink cave to red cave. From freckled arm to eyelash.
Some of us have even returned to Sophie after a foray into Glenn, and the heartiest of us have
traveled back to Glenn yet again. With Sophie we have open borders.
Once, we, Glenn, took a course of penicillin. We had been invaded by an army of streptococci
(yellow, fanged). The penicillin slaughtered most of us, along with the invading army. Our cell
walls disintegrated. We were naked and tender, as vulnerable as amphibian eggs nesting in a
creek bed as the oil spill rainbows nearer, as the mist of Roundup Ready settles over them like
a veil. Countless numbers of us shriveled and died. Dead, we traveled the purple byways of our
body. We coursed through the blue tributaries, rested in the dark brown pools. We joined the
other carcasses for the exodus. Our tiny bodies lay in drifts. For a time, Glenn was sparsely
populated, almost a ghost town. It was a terrible time. But those of us who remained began to
recolonize. We accepted new settlers, begging them off Sophie, off hamburgers, off lettuce and
doorknobs. We were homesteaders as we had never been before.
When we, Glenn, feel sad, many of us become wanderers in the weeping. We become sailors,
adrift on the Sea of Tears, which only bursts its banks occasionally. Our body contains a rust
colored ocean in the lining around our heart. We live on a crust of salt on the surface of our
eyes and in the tunnels of our nose. We rest in the pockets of our skull—we call it The Cave of
Montesino. Sometimes, we get restless. But like Sinbad the Sailor, we vow to stay, stay, stay.
This time, we will remain. We will drift on our homey, stagnant ponds. But just as we settle in,
the tide rises. In a splash, we roll down our cheeks. We encounter exotic foreigners—desert
dwellers used to traveling by wind or fingertip. We come to rest on sleeves or tissues.
Sometimes, we are licked by the swift, broad tongue of the dog. We travel on that meaty sail
until the dog licks the baby, or itself, and then we find new resting places. We set up camp in
waving fields of fur, or on the smooth powdery expanses of a chubby thigh. We stake our claim
in the hot dark crevasse of baby’s elbow.
But we, Glenn, are also raging xenophobes. In particular, we are nervous about silverware in
restaurants. We know that the community in a dishwasher is dense, hostile, and well-fed. Those
fierce creatures scoff at detergents, eating gravy and whatnot, eating each other, dividing and
dividing and dividing. We know that the hands of the workers are wild gardens, too, overrun
with weeds and creepers. We picture their dark rituals, their strong armies, and we quiver. So
when we, Glenn, dine in a restaurant, we bring our own silverware tucked into Sophie’s purse,
sterilized in boiling water and a splash of alcohol, wrapped in starched linen and sealed in a
zip-loc. Sophie sometimes expresses irritation at this practice, but she puts up with it for the
sake of peace. She kisses us, and smoothes our brow. We love it when she smoothes our brow.
Some of us take the opportunity to jump ship. Escaping on the tips of her fine fingers, we
become Sophie.
We take comfort in each other. We, Glenn, tell ourselves that Glenn used to feel lonely, back
when we thought of ourselves as singular, back when we called ourselves “I” and “me.”
How foolish, some of us say, that loneliness, that oversight. But some of us protest: we feel
criticized. Well, we were all so quiet back then, we tell us, and those of us in the mouth dance
and scoot and shuffle like so many Pop Rocks. Gently, we run our index finger along our arm,
gathering a cocktail party in the whorls of our fingertip, and we kiss that fingertip, some of us
leaping from lips to finger, others from finger to lips. We, Glenn, are never alone.
VOLUME 87, N o . 4
THE QUARTERLY REVIEW OF BIOLOGY
DECEMBER 2012
A SYMBIOTIC VIEW OF LIFE: WE HAVE NEVER BEEN
INDIVIDUALS
SCOTT F . GILBERT
Department of Biology, Swarthmore College
Swarthmore, Pennsylvania 19081 USA
Biotechnology Institute, University of Helsinki
00014 Helsinki, Finland
E-MAIL: [email protected]
JAN SAPP
Department of Biology, York University
Toronto, Ontario M3f 1P3 Canada
E-MAIL: [email protected]
ALFRED I. TAUBER
Department of Philosophy, Boston University
Boston, Massachusetts 02215 USA
E-MAIL: [email protected]
KEYWORDS
symbionts, symbiosis, individuality, evolution; holobiont
ABSTRACT
The notion of the “biological individuell” is crucial to studies of genetics, immunology, evolution,
development, anatomy, and physiology. Each of these biological subdisciplines has a specific conception of individuality, which has historically provided conceptual contexts for integrating newly
acquired data. During the past decade, nucleic acid analysis, especially genomic sequencing and
high-throughput UNA techniques, has challenged each of these disciplinary definitions by finding
significant interactions of animals and plants with symbiotic microorganisms that disrupt the
boundaries that heretofore had characterized the biological individual. Animals cannot be considered
individuals by anatomical or physiological criteria because a diversity of symbionts are both present
and functional in completing metabolic pathways and serving other physiological functions. Similarly, these new studies have shown that animal development is incomplete without symbionts.
Symbionts also constitute a second mode of genetic inheritance, providing selectable genetic variation
for natural selection. The immune system also develops, in part, in dialogue with symbionts and
The Quarterly Review of Biology, December 2012, Vol. 87, No. 4
Gopyright © 2012 by The University of Ghicago Press. All rights reserved.
0033-5770/2012/8704-0003?15.00
325
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326
THE QUARTERLY REVIEW OF BIOLOGY
VOLUME 87
thereby functions as a mechanism fcyr integrating microbes into the animal-cell community. Recognizing the “holobiont “—the multicellular eukaryote plus its colonies of persistent symbionts—as a
critically important unit of anatomy, development, physiology, immunology, and evolution opens up
new investigative avenues and conceptually challenges the ways in which the biological subdisciplines
have heretofore characterized living entities.
I
N THE EARLY modern period, mirroring
the appearance of the independent citizen,
the notion of the autonomous individual agent
framed a biology that was organized iiround
the study of particulate, interacting, living entities (Taylor 1989). Anatomical, physiological,
and developmental criteria were conceived
solely in terms of individuals, and tiie Darwinian view of Ufe regarded aggregates of individuals of common ancestry as identifiable units
in competition with one Einother. ‘With the understanding that plants and animals are comprised of living “cells,” a new orientation
quickly developed concerning the integration
of physiological processes and anatomic units,
but still these cells were understood as agents
in constructing and sustaining a singular organism that would in turn maintain its autonomy and integrity. Only witii the emergence of
ecology in the second half of tiie 19th century
did organic systems—comprised of individuals in cooperative and competitive relationships—complement the individual-based
conceptions of the life sciences.
The development of such complex formulations of individuals and systems depends on
myriad fectors, of which technology constitutes
a miijor component in the characterization
process. We perceive only that part of nature
that our technologies permit and, so too, our
theories about nature are highly constrained
by what our technologies enable us to observe.
But theory and technology act on each other
reciprocally: we construct those technologies
that we think are important for examining a
particular perspective of nature. The development of the microscope, for example, revealed
the hitiierto invisible microbial world of bacteria, protists, and fungi; and the descendants
of that instrument further allowed the discovery of subcelltilar organelles, viruses, and
macromolecules. New technologies such as
polymerase chain reaction, high-throughput
RNA analysis, and next generation sequencing
continue to dramatically transform our con-
ceptions of the planet’s biosphere. They have
not only revealed a microbial world of much
deeper diversity than previously imagined, but
also a world of complex and intermingled relatkmships—not only among microbes, but also
between microscopic and macroscopic life
(Gordon 2012). These discoveries have profoundly challenged the generally accepted
view of “individuals.” Symbiosis is becoming a
core principle of contemporary biology, and it
is replacing an essentialist conception of “individuality” with a conception congruent with
the larger systems approach now pushing the
life sciences in diverse directions. These findings lead us into directions that transcend the
self/nonself, subject/object dichotomies that
have characterized Western thought (Tauber
2008a,b).
This reorientation is not new for the microbial or botanical sciences. In the world of protists, hereditary symbiosis, the inheritance of
acquired symbionts is legion. In the microbial
world, “you are what you eat” can be taken
literally. In botanical science, the concept of
the autonomous individual has also been
challenged by discoveries concerning rhizobia, mycorrhizae, and endocytic fungae.
Nonetheless, zoologists long subscribed to a
more individualist conception of the organism, since the role of microbial symbionts
had been more difficult to document in animal evolution (Sapp 1994, 2002, 2009). We
report here that the zoological sciences are
also finding that animals are composites of
many species living, developing, and evolving together. The discovery of symbiosis
throughout the animal kingdom is fundamentally transforming the classical conception of an insular individuality into one in
which interactive relationships among species blurs the boundaries of the organism
and obscures the notion of essential identity.
Our aims in this overview are to: outiine
the data demonstrating that animals are
symbiotic complexes of many species living
DECEMBER 2012
SYMBIOTIC VIEW OF LIFE
together; demonstrate how a thoroughly
symbiotic perspective opens important areas of research and offers fundamentally
new conceptions of the organism; and explore what this new evidence means for
biology, medicine, and for the conservation of biodiversity.
GRITERÍA FOR INDIVIDUALITY
What would biological science be if symbiosis were seen as the rtile, not the exception?
What scientific questions wotald become paramount and how might this change our view of
Life if intimate cooperation between species
were a fundamental feattare of evolution? What
could “individual selection” mean if all organisms were chimeric, and there were no real
monogenetic indi-viduals?
There are many ways in which the term
“individual” is used in biology. Individuals
can be defined anatomically, embryologically, physiologically, immunologically, genetically, or evolutionarily (see Geddes and
Mitchell 1911; Glarke 2010; Nyhart and Lidgard 2011). These conceptions, though, are
not wholly independent of one another. Nor
have these definitions of individuality often
been explicitly articulated as such. Indeed,
even in biology today there is a dearth of
definition in what constitutes the individual
organism. Still, definitions are implied, and
each stems from the common tenet of genomic individuality: one genome/one organism. As such, all classic^ conceptions of
individuality are called into question by evidence of all-pervading symbiosis.
327
resides). When this symbiosis is broken by a
prolonged increase in sea-surface temperatures, corals “bleach.” They lose their algal symbionts and die. Similarly, the entity we call a
cow is an organism whose complex ecosystem
of gut symbionts—a diverse community of celltilose-digesting bacteria, ciliated protists, and
anaerobic fungi—informs its specialized anatomy, defines its plant-digesting physiology, regulates its behaviors, and taltimately determines
its evolution (Kamra 2005).
In addition to the mitochondrial vestiges
of ancient symbiosis, thousands of bacterial
“species” (themselves genetic composites)
live in intimate association with our own
eukaryotic cells. Estimates that 90% of the
cells that comprise our bodies are bacterial
(Bäckhed et al. 2005; Ley et al. 2006) beüe
any simple anatomical understanding of
individual identity. Metagenomic sequencing (Qin et al. 2010) has shown that each
human gut has entered into a persistent pstrtnership with over 150 species of bacteria,
and that the human species maintains about
1000 major bacteria groups in our gut microbiome. TThe gene set contained by this symbiotic metagenome is about 150 times larger
than that of the human eukaryotic genome.
And this does not include the symbionts of
human airways, skin, mouth, or reproductive
orifices.
Mastotermes darwiniensis, a termite of north-
em AtistraUa, may claim the title of “poster
organism” for the chimeric indi-vidual. The
worker termites eat trees and entire homes,
digesting the cellulose in their guts and constructing elaborate subterranean nests. But as
Lewis Thomas (1974) and Lynn Margtilis and
ANATOMICAL INDIVIDUALITY
Dorion Sagan (2001) have asked: What constiAnatomically, the individual animal is re- tutes the indi-vidual organism? How can a
garded as a structured whole. Yet, data fi^om worker termite be considered an indi-vidual
PGR show that the cells and bodies of animals when it is the hive that is the reproductive imit
are shared with numerous “species” of bacteria of the species, and the worker carmot even
and other microbes. In some sponges, nearly digest cellulose without its gut symbiont, Mix40% of the volume of the organism is com- otricha paradoxa, which is itself a genetic comprised of bacteria, which contribute signifi- posite of at least five other species? Neither
cantly to host metabolism (Taylor et al. 2007). humans, nor any other organism, can be reThe algal symbiont, Symhwdinium, provides up garded as individuals by anatomical criteria. To
to 60% of the nutrients needed by its host coral capture this complexity, the term “holobiont”
(the term “host” is used here in the classical has been introduced as tbe anatomical term
sense to denote the larger, eukaryotic, multi- that describes tbe integrated organism comcellular organism in which the “symbiont” prised of both host elements and persistent
328
THE QUARTERLY REVIEW OF BIOLOGY
populations of symbionts (Rosenberg et al.
2007).
DEVELOPMENTAL INDIVIDUALITY
The deuebpmmtal view of animal individuality was originally proposed by Thomas Huxley
in his published lecture, “Upon Animal Individtiality” (Huxley 1852). Avariant of the anatomical version of biological individuality, the
individual animal proposed here is understood
to be that which proceeds from ovum to ovum.
Yet, this view of life is belied by evidence that
what we understand to be the “individual” develops as consortia of animal cells and microbes (McFall-Ngai 2002; Gilbert and Epel
2009; Fraune and Bosch 2010; Pradeu 2011).
Indeed, the development of both vertebrates
and invertebrates (especially larval and postembryonic development) is predicated on intimate relations with microbes.
In some instances, tiie symbiosis may be parasitic, one organism benefiting at the expense
of another. For example, the development of
the European blue butterfly Macidinm arum
requires that the female lays her eggs on thyme
plants. The larvae, however, do not eat thyme,
but drop to the ground, where they produce a
mixture of volatile chemicals mimicking the
smell of the larvae of the ant species Myrmica
sabukti Patrolling Myrmicae mistake the butterfly larva as one of tiieir own, and cany it into
the ant nest Once in the nest with the ant
larvae, the caterpillar is fed by the workers,
eventually eating yoting ants until it is ready to
pupate. It undergoes metamorphosis in the
ant colony and emerges as an adult (Thomas
1995; Nash et al. 2008). This type of life-cycle
symbiosis occurs throughout marine invertebrates, where larvae require cues, often from
their food sources, in regard to where and
when to settle and undergo metamorphosis.
The importance of symbiotic organisms
for the completion of host life cycles is also
evident in parasitic worms, where bacteria
are crucial for embryogenesis and molting
(Hoerauf et al. 2003; Goulibaly et al. 2009)
and in salamander development, where
symbiotic algae on the egg jelly produce
the oxygen necessary for the survival of the
spotted salamander embryos (Olivier and
Moon 2010; Kerney et al. 2011).
In numerous organisms, the develop-
VOLUME 87
ment of particular organs is predicated on
chemical signals from symbionts (Douglas
1988, 2010). For example, the ovaries of
the parasitoid wasp, Asobara, undergo apoptosis if signals from their Wolbachia symbionts are lacking (Pannebakker et al. 2007).
And the newborn of the squid Euprymna
scolopes lacks a light organ, which is developed in cooperation between the squid
and the luminescent bacteria ( Vibrio fisheri)
absorbed by its ventral epithelium (McFallNgai et al. 2012). Without the bacteria, the
organ does not develop.
In “germ-free” asymbiotic mice, the development of the immune system and the
digestive system cannot be completed without gut bacteria (Ley et al. 2006, 2008; Lee
and Mazmanian 2010). Rather, these mice
have insufficient intestinal capillaries, poorly
developed or absent gut-associated lymphoid
tissue, and a diminished T-cell repertoire
that gives them an immunodeficiency syndrome (Stappenbeck et al. 2002; Rhee et al.
2004; Mess et al. 2008; Duan et al. 2010). In
zebrafish, microbes regulate (through the
canonical Wnt pathway) the normal proliferation of the intestinal stem cells. Without
these microbes, the intestinal epithelium has
fewer cells, and it lacks goblet cells, entroendocrine cells, and the characteristic intestinal brush border enzymes (Rawls et al. 2004;
Bates et al. 2006).
Microbial symbionts appear to be a normal and necessary part oJF the life cycle of
all mammals, which acquire the microbes
as soon as the a …
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