The Adaptive Bleaching Hypothesis

[FAUTIN DAPHNE G]

Dear Coral-Listers,

I am taking this opportunity to respond to several recent messages
concerning the Adaptive Bleaching Hypothesis (ABH) that was proposed by
Bob Buddemeier and me, and then modeled by John Ware, with input from us.
I helped formulate the ABH because I am eager to understand the symbioses.
I am writing now because I perceive some of the recent exchanges
ostensibly concerning the ABH deal with matters that are not part of the
ABH and thus do not advance that understanding.

The ABH was our deduction from experimental results and empirical
observations that had been published at the time we developed it; those
data and what they contributed to the ABH are detailed in our
publications.  Thus it is not true, as one lister recently asserted, that
there is no evidence for the ABH.

The writers of some recent messages seem to regard the ABH more as a law
than a hypothesis.  In framing it as "a testable hypothesis," we
recognized that additional data could prove to be inconsistent with our
inferences about the workings of zooxanthellae symbioses, entirely or in
part.  Thus, in the manner that science works, falsification would result
in more refined hypotheses being advanced and tested, gradually improving
our understanding of the symbioses.  In a recent message in which he
claimed falsification of some of the five critical assumptions of the ABH,
Hoegh-Guldberg advocated "discarding" the ABH.  What I seek in combination
with data that are truly inconsistent with the ABH are second-generation
hypotheses that take into account the new data - using the parts of the
ABH that work, and substituting for the unworkable parts.  More
importantly at this juncture, I am not persuaded that those assumptions
have been falsified.

The ABH was not meant to apply to every instance of bleaching.  By way of
analogy, that natural selection is not the only selective force in
evolution does not falsify natural selection.  To take one clear example,
some stresses that result in bleaching are lethal, to some or all the
bleached corals, and so, obviously, the ABH is irrelevant in such
instances.  This is why we confined the models of Ware et al. to
non-lethal stresses.  (Hoegh-Guldberg correctly inferred this is not an
assumption of the ABH but a condition under which the model was run, so I
am puzzled why he even raised it; it is irrelevant to the substance of the
ABH.)

We did propose "that bleaching is not merely pathological, but is also
adaptive, providing an opportunity for recombining hosts and algae to form
symbioses better suited to altered circumstances" (Ware et al. 1996).  We
also recognized that the organisms might be unable to take advantage of
such an opportunity.  For example, even with sublethal stresses, in places
with low zooxanthellae diversity, a new combination would be unlikely. And
superior combinations might not form by chance, for the hypothesized
recombination is a stochastic - not a deterministic - phenomenon.  We also
explicitly stated that the ABH applies to the level of bleaching under
which the symbiosis evolved -- what has been considered "background" - and
that a mechanism that evolved under that level may not be adaptive if what
we are now experiencing is as unprecedentedly severe and widespread as
some believe (which is consistent with what Hoegh-Guldberg reported has
been found in Japan).

The "replacement" zooxanthellae, according to the ABH, can be either
exogenous or endogenous.  At the time we formulated the ABH, an endogenous
source was thought by many experts to be impossible, since it was then
considered that any cnidarian polyp or colony would harbor only one
"strain" of zooxanthellae.  We inferred from the published literature that
"strains" could coexist, and so saw a proliferation of one "strain" at the
expense of another to be a possible response to altered circumstance.  We
now know that multiple "strains" can coexist.  Thus the comment that
"Baker (2001)  cannot say that the new bands are due to invasion of
external zooxanthellae or a case of up-regulation of a small existing
population of the particular type of zooxanthellae concerned" is not
germane to the ABH - either alternative supports it.  The exogenous source
is the surrounding water, and therefore ultimately are zooxanthellae in
their free-living stage or those were released under stress.  Whether
those that leave in the bleaching process are viable, much less infective,
was raised in the original publication as a matter to be investigated; it
has not, to our knowledge, been resolved.  Thus criticisms such as that of
Hoegh-Guldberg (1999), "The key observations that corals, when heat
stressed, expel one variety of zooxanthellae and take on another more
heat-tolerant variety while the heat stress is still present, has never
been made," misrepresent the ABH and thus do not test its tenets.

The preceding quote and several recent list messages have focused on
thermal bleaching.  This is not a requirement of the ABH, which was
proposed to operate as a result of any stress or combination of stresses
that provoke bleaching.

Hoegh-Guldberg began a recent message with 'a clarification with respect
to the biological terms "adaptation" and "acclimation."' I am uncertain
how this comment relates to the debate.  We have tried to be consistent in
application of those terms - see papers in the recent "American Zoologist"
volume concerned with how coral reefs adapt, acclimate, and acclimatize
(especially that of Gates).  Hoegh-Guldberg's definition of adaptation as
"genetic changes in a population that lead to genetically based
characteristics of that population considered more optimal with respect to
the local environment" is the sense in which we created the ABH.  For we
explicitly regard the zooxanthella-host complex as an ecological entity
that is not the sum of its parts (an additive model was used by Ware et
al. to be mathematically tractable, but its departure from our concept was
made explicit).  Thus, in the ABH, under identical circumstances, a
species of coral with one "strain" of zooxanthellae might be maladapted
but well adapted with another.  This seems to be substantiated in patterns
of "strains" of zooxanthellae that live in shaded and lighted portions of
a single coral colony, and of "strains" of zooxanthellae that live in
shallow and deep colonies of a single species of coral.  Part of the
decision on whether to use the pigeon-hole "adaptation" or "acclimation"
that Hoegh-Guldberg raises may depend on one's concept of who is "in
charge" in the symbiosis - if the animal is making a selection, it may be
nearer the "acclimation" end, whereas if the zooxanthella is choosing a
suitable home, it may be nearer the "adaptation" end.

In his message, Hoegh-Guldberg disputed the mutability of
host-zooxanthella combinations on the time scale required for the ABH to
operate.  Our inference that the change could happen was based on
experiments such as those of Fitt cited by Hoegh-Guldberg, who stated "To
my knowledge, no lab or field infection experiment using dinoflagellates
from other hosts (like those of WK Fitt and others) have ever resulted in
a new combination of symbiotic algae and host."  In fact, we interpreted
Fitt's data (and those of Kinzie and Chee) as showing that new
combinations could be established in short order - although allochthonous
zooxanthellae did not establish in all hosts, some did so temporarily, and
others remained longer.  Hoegh-Guldberg continued "In cases where foreign
types of zooxanthellae were introduced, populations were eventually
replaced by the original type of zooxanthellae."  As we wrote in the
original BioScience paper, because the scientists controlled conditions to
minimize stress on their experimental subjects, those experiments were
conducted under laboratory conditions that were known to be suitable for
the subjects - which are those in which the "native" zooxanthellae-host
combination is favored.  Thus a reversion to the pre-existing combination
is precisely what would be predicted by the ABH.  The recently published
experiment by Baker put corals into situations that persisted - and his
results are also consistent with the ABH.

Hoegh-Guldberg's comment "Also - no one has seen a change in the types of
zooxanthellae occupied by a coral following a bleaching event (i.e. new
combinations arising from a bleaching event)" is beside the point in the
debate over the ABH for several reasons.  I stated one above - unless the
stress that produced the bleaching persists, the pre-existing combination
will be favored, so no change is to be expected.  A practical one is being
able to know what the situation was before the stress and what it is
afterward.  For we are searching for changes in an entity that, until very
recently, was viewed by most people as unitary (that is, there was one
"strain" of zooxanthellae) and we do not yet know the extent of the
diversity because we do not yet know what differences might exist.  Part
of our proposing the hypothesis was to encourage scientists to find ways
to distinguish the members of this all-important symbiosis, individually
and in combination.  Moreover, the ABH does not require that every
"strain" of zooxanthellae be capable of living in every host species - we
explicitly modeled the ABH on there being generalists and specialists on
both sides of the symbiosis (just as there are anemonefish and host sea
anemones - in the former case belonging perhaps to two genera, in the
latter certainly to three families).  I, for one, do not "think of
transferring zooxanthellae between hosts as partly akin to transplanting
chloroplasts or mitochondria between plant species" - a bit of evidence
that clearly shows zooxanthella symbiosis is a less well integrated one is
the phenomenon of bleaching itself.  The possibilities Hoegh-Guldberg
raises with the comment "the types of zooxanthellae that occupy different
corals are quite separate genetically and may represent different species
or even genera (Trench, McNally et al. 1994 and others) - hence are likely
to have a large suite of different requirements and features that have to
be integrated (evolved) in order for a symbiosis to function.  Adopting
life within another cellular environment is not trivial and may involve
many coordinated changes in genetic makeup" provide grist for
investigation, but do not constitute falsification of the ABH.

We inferred that "stress-sensitive combinations have competitive
advantages in the absence of stress, which implies a reversion to
stress-prone combinations under non-stressful conditions" to account for
the continued existence of combinations that are vulnerable to conditions
that recur (such as the annual bleaching Jokiel and others found in
Hawaii, and that Fitt has more recently documented in Florida). Otherwise
the system would be ratcheted to increasingly stress-resistant
combinations with a time course that would seem too rapid for any other
known mechanism.  Using this assumption, Ware was able to create a model
that bears remarkable resemblance to the time course of actual bleaching
events.

I look forward to advancing understanding of bleaching and its
consequences though well-crafted experiments that are published in the
peer-reviewed literature.


Sincerely,
Daphne G. Fautin
Professor, Ecology and Evolutionary Biology
Curator, Natural History Museum and Biodiversity Research Center
Haworth Hall
University of Kansas
1200 Sunnyside Avenue
Lawrence, Kansas 66045-7534  USA

telephone 1-785-864-3062
fax 1-785-864-5321
for e-mail, please use fautin at ku.edu

lab web page: www.nhm.ku.edu/~inverts

direct to database of hexacorals, including sea anemones, released
                           12 July 2001 
           *** http://www.kgs.ku.edu/Hexacoral/Biodata/ ***

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