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First published online January 16, 2009
Journal of Experimental Biology 212, 446-451 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025916
Review |
Insect homeostasis: past and future
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
e-mail: shpm100{at}hermes.cam.ac.uk
Accepted 12 November 2008
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Summary |
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 TOP Summary Control of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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Key words: Malpighian tubule, diuretic hormones, ions and water, epithelial transport, fluid secretion, transport of organic compounds
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Control of haemolymph volume in fed Rhodnius |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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). It then greatly
accelerates the action of several systems that together allow it to rid itself
of the surplus fluid and ions contained in the meal by transporting them out
of the midgut into the haemolymph and then out of the haemolymph in the urine
produced by the Malpighian tubules. This is done at a huge rate. The
Malpighian tubules secrete approximately 1000 times faster when they are
hormonally stimulated on the occasion of the meal
(Maddrell, 1963). A fed Rhodnius is capable of excreting its own unfed body mass every forty minutes or so. That means that a volume of fluid equal to that of the entire haemolymph volume passes through the haemolymph every 10–15 min as it is transferred from midgut to haemolymph and then from the haemolymph out of the insect via the Malpighian tubules. One might think that the relatively small amount of haemolymph would be overwhelmed by this and would be in danger of big changes in volume and composition. But in fact the haemolymph is relatively little affected.
Perhaps the most interesting problem in Rhodnius has to do with how the rate of fluid flow into the haemolymph from the midgut is matched by the rate of fluid flow out of the haemolymph via the Malpighian tubules. In other words, how is the haemolymph volume protected against the potentially embarrassingly large changes in volume that would occur were these two fluid flows not matched?
I previously suggested that this matching might be achieved if the midgut
was less sensitive to a circulating diuretic hormone than the Malpighian
tubules (Maddrell, 1977). In
addition, I suggested that the maximal rate of stimulated fluid transport by
the midgut must be higher than the maximal rates of fluid secretion by the
four Malpighian tubules. Since that time, it has been found that there are at
least two hormones released into circulation to control these fluid transport
processes (Lange et al., 1989;
Maddrell et al., 1991a).
Nonetheless, a composite figure for the response of the midgut and Malpighian
tubules to the hormones might be as shown in
Fig. 1. The curves have to be
drawn rather more steeply than if the epithelia were being stimulated by a
single hormone because this is one of the effects of synergism between the, at
least, two diuretic hormones released after feeding
(Maddrell et al., 1993).
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What is the evidence to support this proposal? |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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). The
midgut is less sensitive to 5-HT than the Malpighian tubules are
(Farmer et al., 1981). If we
then suppose that the midgut can transport fluid faster than can all four
Malpighian tubules, we have the basis for an automatic matching of their rates
when both are stimulated by this hormone. There is no direct evidence for this
but it is fairly easy to believe, as one can calculate that the area of the
midgut epithelium is approximately 8 times larger than the total area of the
fluid-secreting parts of the four Malpighian tubules (admittedly this ignores
the fact that both tissues have extensive elaborations of their basolateral
and apical membranes and they may differ in the extent of this). It follows
that the rate of fluid transport across a unit area of midgut epithelium is
considerably lower than that of the Malpighian tubules when both are
transporting at the same overall rate.
One method of obtaining hormones from their release sites is to treat the
sites with K+-rich saline
(Maddrell and Gee, 1974). This
was done with the mesothoracic ganglionic mass and its abdominal nerves
– the release sites for the diuretic hormones. The hormone-rich saline
was then tested on the midgut and the Malpighian tubules from the same insect
as used to prepare the test saline. The results showed that the Malpighian
tubules are 2–3 times as sensitive to the hormone-laden saline than is
the midgut wall. So this aspect of the proposed relation shown in
Fig. 1 has support.
Rather similarly, it can be shown that the haemolymph of recently fed
insects always contains hormone concentrations more than enough, by
approximately 2–3 times, that are required to elicit the maximal rate of
fluid secretion by the Malpighian tubules. So if the Malpighian tubules are
maximally stimulated in the intact fed insect, the rate of diuresis should be
more or less constant – and it is
(Maddrell, 1964).
By contrast, testing haemolymph samples from fed insects on isolated
midguts usually produced little effect. However, we know that target tissues
can inactivate hormones. Early on, I showed that samples of haemolymph from
fed Rhodnius lose their diuretic activity much more rapidly if they
bathe a Malpighian tubule than if they are merely left by themselves
(Maddrell, 1964). In addition,
we would expect from the model that the haemolymph hormone concentration
should only be sufficient partially to stimulate the midgut. So it is credible
to suppose to that hormone-rich haemolymph taken from a fed Rhodnius
would be sufficiently rapidly inactivated by the midgut epithelium to prevent
its having much effect on that epithelium, especially given the large surface
area of the midgut.
And of course we already know that 5-HT affects the Malpighian tubules at concentrations too low to affect the midgut.
Further support for the model comes from some experiments not previously published. In these experiments, I removed Malpighian tubules from a series of 5th stage Rhodnius leaving some with three Malpighian tubules, others with two Malpighian tubules and some with only one. Then when these insects were fed blood meals, not surprisingly the rates of diuresis were, respectively, cut by 25%, 50% or 75% (Fig. 2). And diuresis lasted 50% longer, twice as long or 4 times as long, respectively. But what was as interesting was that the volume of haemolymph did not appear to change to any marked degree. Because the plasticised and extended abdominal endocuticle is more or less transparent, one can illuminate the insect from below and clearly see how much haemolymph there is outside the midgut.
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) –
unlike Malpighian tubules, where unstimulated tubules secrete fluid
100–1000 times as slowly as they do when maximally stimulated. So if the
midgut transport rate in a fed insect with only one Malpighian tubule is
higher than the maximal rate of fluid secretion by that single Malpighian
tubule, it will overwhelm transport by the Malpighian tubule, the haemolymph
volume will rapidly increase and the Malpighian tubule will shut down as the
hormone concentration becomes insufficient to stimulate it. And, indeed,
observation of such insects shows that they have greatly increased volumes of
haemolymph.
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So in Fig. 3 we have a working model to explain how the rates of fluid flow into the haemolymph can be matched to the outflow almost regardless of how fast the Malpighian tubules secrete fluid. In this way, the insect is protected against large changes in volume of haemolymph from any shortfall in fluid secretion by its Malpighian tubules.
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Other general problems with insect hormones |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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).
So there is a general problem of how insects can assess the level of hormones
in circulation. Perhaps the easiest solution would be if the releasing sites
(the neurohaemal areas for neurohormones) were themselves directly sensitive
to the concentrations in circulation of the hormones they release. As far as I
know, this has yet to be looked at.
Another problem concerns the apparently over-large number of hormones that can act on Malpighian tubules – and, it can be imagined, on other organs, such as the heart.
The fact that many different hormones affect fluid secretion by Malpighian
tubules had been known for some time [see paper by Coast in this issue
(Coast, 2009)]
(Donini et al., 2008). There is
evidence for the Malpighian tubules of Manduca sexta that at least
eight different sorts of compounds can significantly affect the rates of their
fluid secretion (Skaer et al.,
2002). All the substances tested on the Malpighian tubules also
accelerated the rate of heartbeat in Manduca and at similar
concentrations.
What is one to make of this? What we said at the time was `we suggest that there may exist in the extracellular fluid a continuous broadcast of information in the form of a chemical language, to which many or all parts of the body continuously respond on a moment-to-moment basis and which, because of the greater information in it, ensures a more effective and efficient coordination of function than could be achieved by a series of single, tissue-specific hormones that force stereotypical responses by their target tissue(s)'.
And indeed this idea may explain the apparently overly complex array of hormonal signals affecting such processes as moulting in insects where many hormones contribute to varying degrees. If it is the case that events in an animal are at least partly controlled by an internal language with a rich array of `words' (each a circulating chemical signal), then this complexity should not be surprising but should be expected.
It is consistent with these ideas that a hormonal signal is not a command but merely a signal to which a tissue or cell may or may not respond. So, for example epidermal cells in an insect may respond to the appearance of 20-HE in circulation by moulting the cuticle above them. Other cells respond quite differently, with many of them content to ignore the signal completely. Similarly, the appearance of bursicon in circulation is read by most cells in the developing wings of, say, a dipteran fly as notice that they should undergo programmed cell death and disappear completely so as to lighten the resulting wing. Other cells, even some of those in direct contact with the dying cells, remain unaffected. These undisturbed cells line the haemolymph spaces in the wing veins and they need to be able to continue to carry out their normal functions. So, apparently very similar cells respond completely differently to the same hormone regime – as one would expect if hormones were only elements in a supply of information to the tissues of the body.
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Possible differential sensitivity of Malpighian tubule cells to hormones |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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).
A useful peculiarity of Rhodnius' Malpighian tubules might allow
single Malpighian tubule cells to be assessed directly. A few percent of
Rhodnius' Malpighian tubules have an abnormality in which a single
upper Malpighian tubule cell appears among the first few cells of the lower
Malpighian tubule (Fig. 4)
(Maddrell and Overton, 1985).
The whole Malpighian tubule can then be set up in a way that allows the
physiological properties of the single cell to be examined
(Fig. 5). For example one can
measure the transport of sodium ions into the lumen
(Fig. 6). As this figure shows,
the sodium transport by one upper Malpighian tubule cell is very large and
very easy to measure. It should be quite simple to construct a dose/response
curve to a particular stimulant for that single cell. And if one first did a
dose/response curve for the entire upper Malpighian tubule upstream, the two
dose/response curves could be compared. In a few cases, more than one upper
Malpighian tubule cell appears distant from its fellows, so the sensitivity of
each could be studied. If they are in contact with each other, one could then
investigate whether being in contact affects their hormone sensitivity.
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Oscillations in trans-epithelial potential difference in isolated Malpighian tubules |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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)
after which the lumen holds a near constant negative potential difference with
respect to the bathing medium. Here, I report an unusual occurrence in which
Rhodnius' upper Malpighian tubules stimulated with 5-HT showed a TEP
that started to oscillate (Fig.
7). The size of the oscillations would grow until they were maybe
20 mV or more in size – then they faded away. What was striking was how
regular the oscillations were. What appeared to cause this sort of behaviour
was if the Malpighian tubule was rather bunched up and crowded at one side of
the bathing drop. Indeed, the oscillations could be stopped by moving the
Malpighian tubule until it was more central in the bathing drop and less
bunched up. Or if more, fresh saline was added, that too would often stop the
oscillations.
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The oscillations were very temperature sensitive. If the dish in which the experiment was going on was warmed, the oscillations would get faster and indeed bigger. And the frequency of oscillation was so predictable that one could assess the temperature of the bath surrounding the Malpighian tubule in its drop of bathing fluid from the periodicity or wavelength of the oscillations. The log of the interpeak time was more or less linearly related to the temperature over the range from 20–32°C (Fig. 8).
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If we are to see what underlies the oscillations, we need to know what the various ion movements are and what are the electrical potential differences that they might cause. And, also, how variations in cellular second messengers affect potential differences. Unfortunately, we also need to know which of these is the most sensitive to oxygen change, if indeed that is the physiological factor that precipitates these nice oscillations. Given the predictability of the response and its size, it might be possible to find out what is the proximate cause of the oscillations. More usefully, however, these oscillations might be useful in a deeper understanding of the cellular responses to stimulation.
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The future |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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; Maddrell and
Phillips, 1975). And some Malpighian tubules can transport calcium
ions (Herbst and Bradley, 1989;
Maddrell et al., 1991b). A
wide range of organic materials is also known to be actively transported by
Malpighian tubules. There are early references to their ability to concentrate
different sorts of dyes (Lison,
1937) but they are also able to transport cardiac glycosides
(Rafaeli-Bernstein and Mordue,
1978), alkaloids (Maddrell and
Gardiner, 1976), uric acid
(Wigglesworth, 1931;
O'Donnell et al., 1983),
salicylate (Ruiz-Sanchez et al.,
2007) and compounds related to para-amino hippuric acid
(Maddrell et al., 1974). And
there is something known of how such transport of organic materials is altered
by the insect in response to the presence of absence or abundance in the food
material or the physiological state of the insect
(Maddrell and Gardiner, 1975;
O'Donnell et al., 1983). But
by comparison with what is known of ion and water transport, these very
important aspects of Malpighian tubule function have been relatively little
explored. With the new developments in genomics, proteomics and what has been
termed metabolomics, things are certain to change
(Kamleh et al., 2008) [and see
paper by Dow in this issue (Dow,
2009)]. And it is likely that there will be surprises. One major
one has already appeared. Who could have guessed that Malpighian tubules would
be centrally involved in the immune response of insects to xenobiotics
(McGettigan et al., 2005) [and
see paper by Dow in this issue (Dow,
2009)]!
I think we can look forward in the next few years to a greatly increased knowledge of all aspects of insect homeostasis. Exciting times lie ahead!
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References |
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TOPSummaryControl of haemolymph volume...What is the evidence...Other general problems with...Possible differential...Oscillations in trans-epithelial...The futureReferences |
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70–80 µm in diameter. [From
Maddrell and Overton (Maddrell and
Overton, 1985
