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Journal of Neuroscience, Vol 5, 2290-2300, Copyright © 1985 by Society for Neuroscience
Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis
JC Weeks and JW Truman
The metamorphosis of insects is controlled by the blood titers of a small
number of developmental hormones including a class of steroids, the
ecdysteroids. We have studied the developmental fates of several muscles
and their motoneurons during the larval-pupal transformation of the tobacco
hornworm, Manduca sexta. The endocrine events which trigger pupal
development are first, a fall in the blood titer of juvenile hormone,
followed by two subsequent elevations of blood ecdysteroids. The small
"commitment pulse" of ecdysteroids commits tissues to pupal development,
whereas the sustained "prepupal peak" causes the new pupa to be formed
(Riddiford, L. M. (1980) In Progress in Ecdysone Research, J.A. Hoffmann,
ed., pp. 409-430, Elsevier/North-Holland Biomedical Press, Amsterdam). In
the present experiments we were able to correlate specific aspects of the
changing blood steroid titers with the degeneration of larval muscles, and
with the dendritic regression and death of their motoneurons. The abdominal
prolegs, which are the principal locomotory appendages of the caterpillar,
are lost during the larval-pupal transformation. We have followed the fates
of a proleg retractor muscle, PPRM, and its single motoneuron, PPR. Two
other differently fated abdominal muscles not associated with the proleg
were also studied. Surgical and endocrinological manipulations showed that
PPRM degenerates in response to the rising phase of the prepupal
ecdysteroid peak and that interactions with its motoneuron are not involved
in the muscle's death. Motoneuron PPR responds to the rising prepupal peak
by first reducing its dendritic arbor by 40% and then dying. Other proleg
motoneurons regress but do not die, indicating that dendritic regression is
programmed separately from neuronal death. Neither the dendritic reduction
nor the death of PPR involves interactions with its target muscle. These
results indicate that ecdysteroids have independent and parallel effects in
the periphery, where they cause muscle degeneration, and in the central
nervous system, where they cause dendritic regression and death of
motoneurons.
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