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Invertebrate Endocrinology

Matthew Landau, William J. Biggers, Hans Laufer

10.1002/cphy.cp130218

Source: Supplement 30: Handbook of Physiology, Comparative Physiology

Originally published: 1997

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Growth and Morphogenetic Factors
1.1 Insects
1.2 Crustaceans
1.3 Molluscs
1.4 Other Invertebrates
2 Regenerative Factors
2.1 Crustaceans
2.2 Insects
2.3 Cnidarians
2.4 Platyhelminths
2.5 Annelids
2.6 Echinoderms
2.7 Others
3 Pigmentary Factors
3.1 Crustaceans
3.2 Insects
4 Osmoregulatory Factors
4.1 Factors that May Increase Osmotic Pressure
4.2 Factors that May Decrease Osmotic Pressure
5 Metabolic Factors
5.1 Biogenic Amines
5.2 JHs and Farnesylacetone
5.3 Adipokinetic Hormones and RPCH
5.4 Crustacean Hyperglycemic Hormones
5.5 Other Metabolic Factors
6 Reproductive Factors
6.1 Flatworms, Nemertines, and Nematodes
6.2 Molluscs
6.3 Crustaceans
6.4 Insects
6.5 Other Arthropods
6.6 Annelids
6.7 Echinoderms
7 Behavioral Factors
7.1 In Vitro Studies
7.2 In Vivo Studies
7.3 Pheromones
8 Summary
Figure 1. Figure 1.

Chemical structures of ecdysteroids.

From Sakurai and Gilbert 1189, reprinted with permission of Springer‐Verlag, Inc
Figure 2. Figure 2.

Chemical structures of JH‐like compounds.

From Laufer and Biggers 796, reprinted with permission of Peeters Press, Inc
Figure 3. Figure 3.

Blood hormone titers during metamorphosis in Manduca. Time in days. IV‐L, fourth larval instar; V‐L, fifth larval instar; P, pupa; DA, developing adult; A, adult; E, ecdysis (the shedding of the old cuticle); CP, commitment pulse; PP, prepupal peak. Hormone titers are from Bollenbacher et al. 122 and Riddiford 1138. Peak blood ecysteroid titers during the commitment pulse and prepupal peak are (in 20E equivalents) 0.07 and 1.5 μg/ml, respectively, and the maximum value during adult development is 3 μg/g fresh weight 122.

From Weeks and Truman 1442. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc
Figure 4. Figure 4.

Schematic diagram illustrating the control of molting and metamorphosis in the tobacco hornworm moth.

From Gilbert 466 and Gilbert and Goodman 467, reprinted with permission of Sinaver Associates, Inc
Figure 5. Figure 5.

JH titer in the hemolymph of adult female Leptinotarsa decemlineata reared under different photoperiods. Upper graph: GU, Galleria units, after de Wilde et al. 307. Lower graph: measured by gas chromatography/mass spectrometry. LD, long day; SD, short day.

From de Wilde 305. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc
Figure 6. Figure 6.

Extirpated Y‐organ of Orconectes limosus; c, thin cutile, separating the Y‐organ from the branchial chamber; arrow: basement membrane of individual lobule; bs, blood sinus. Azan stain, paraffin section.

From Keller and Willig 709, reprinted with permission of Springer‐Verlag and R. Keller
Figure 7. Figure 7.

Major endocrine and neuroendocrine structures of generalized female Crustacea. Included are the organs important for female reproduction, the eyestalk, sinus gland X‐organ, the mandibular organ, Y‐organ, and thoracic ganglion.

From Laufer et al. 802
Figure 8. Figure 8.

Control (c) stages III and IV, and eyestalkless (es–) stages IVa, IV', and IV that result from eyestalk ablation in stage II.

From Charmantier et al. 197, reprinted with permission
Figure 9. Figure 9.

Radiochromatogram on HPLC system 2(a) of an aliquot of the 100% methanolic silicic acid column fraction from Nereis diversicolor after injection of [3H]ecdysone and maintenance for 24 h. Fractions were collected every 30 s for scintillation counting. The positions of authentic ecdysone (I), 20‐hydroxyecdysone (II), 20‐hydroxyecdysone‐22‐phosphate (V), 20‐hydroxyecdysone acid (VI), ecdysone‐22‐phosphate (VII), and ecdysonic acid (VIII) are shown.

From Mercer et al. 914, reprinted with permission
Figure 10. Figure 10.

Example of simple tissue repair. Penaeus monodon female showing completely healed right eye after ablation; left eye has been tagged for rematuration experiments.

From Primavera 1078, reprinted with permission
Figure 11. Figure 11.

Distribution of ganglion cells (circles) and epidermal sensory cells (triangles) in the tentacles and hypostome. One tentacle is shown in full, while others have been truncated.

From Bode et al. 108, reprinted with permission of American Zoologist
Figure 12. Figure 12.

Experiment illustrating the conversion of FLI‐ to FLI + neurons during head regeneration. Circles and triangles represent FLI+ ganglion and FLI+ epidermal sensory cells, respectively. HU, hydroxyurea; NM, nitrogen mustard; FLI, FMR Famide‐like immunoreactivity.

From Bode et al. 108, reprinted with permission of American Zoologist
Figure 13. Figure 13.

Platynereis dumerilii, posterior regenerates. Photomicrographs of live specimens a: Typical caudal regenerate grown under the hormonal control of an intact prostomium. The endocrine status of prostomia of experimental animals which exhibited this type of regenerate was designated “active.” b: Atypical posterior regenerate developed under nonhormonal conditions. The endocrine status of prostomia of experimental animals exhibiting this type of regenerate and showing epitokoid development was designated “inactive.” Note rudimentary parapodium (arrow) and digitiform outgrowths of the pygidium, typical for the epitokous males, which evacuate sperm. 1, Parapodium of former wound segment; 2, regenerated pygidium; 3, urite (appendage of pygidium); 4, parapodium of regenerated segment.

From Hofmann 577,578, reprinted with permission
Figure 14. Figure 14.

Regeneration in snails with one cerebral ganglion removed was evaluated upon death 2 to more than 24 months after the lesion. Results were arbitrarily grouped into four time periods. The state of repair was categorized as no communication through the side of the missing ganglion (N), tract stage (T), bud stage (B), or ganglion stage (G). Distribution within these four categories was plotted as percent of the total number (n) of animals examined in each postoperative time period.

From Moffet and Ridgway 926. Reprinted with permission of American Zoologist
Figure 15. Figure 15.

The eyestalk of Palaemon serratus showing sites immunopositive for antiadipokinetic hormone sera, which can be used to detect red pigment–concentrating hormone.

From Bellon‐Humbert et al. 57, reprinted with permission of Biological Bulletin, LG, lamina ganglionaris; ME, medulla externa; MI, medulla interna; MT, medulla terminalis; MEX, medulla externa of X‐organ; MTGX‐1 and −2, medulla terminalis of X‐organs 1 and 2; OB, organ of Bellonci; SG, sinus glands; +, neurosecretory cells
Figure 16. Figure 16.

Diagrammatic composite decapod crustacean illustrating neuroendocrine centers (1, eyestalk system; 2, brain; 3, thoracic ganglion; 4, pericardial organ) and osmoregulatory sites (5, stomach; 6, intestine; 7, gill; 8, antennal gland; 9, intracellular).

From Kamemoto 678, reprinted with permission of American Zoologist
Figure 17. Figure 17.

Methyl farnesoate (MF) synthesis varies with embryonic development, which itself reflects ovarian growth.

From Laufer et al. 799, reprinted with permission. Copyright © 1987 by the American Association for the Advancement of Science
Figure 18. Figure 18.

Histological section of androgenic gland implant recovered from masculinized female. Arrows, androgenic gland; v, muscle of vas deferens. Bar = 100 μm. Androgenic glands from Procambrus males recovered after transplantation into females for 326 days.

From Nagamine and Knight 961, reprinted with permission
Figure 19. Figure 19.

Diagrammatic representation of the composite effects of JH in species whose vitellogenesis depends on JH‐controlled vitellogenin synthesis.

From Engelmann 363,364. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc
Figure 20. Figure 20.

Model for control of egg development in Aedes aegypti. EDNH, egg development neurosecretory hormone.

From Hagedorn 517. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc
Figure 21. Figure 21.

Alternative reproductive cycles of Heteropeza pygmaea (Diptera, Cecidomyiidae). Larva (L) derived from the egg (E) develops into pedogenetic female “mother larva” (M♀) producing undetermined daughter larvae (TL). Each daughter larva may become either a female mother larva, a female “imago‐larva” (IL♀), a male mother larva (M♂), and/or a mother larva with mixed progeny (M♀♂). P, pupa; I, imago.

From Weber 1436 and Sehnal 1239. Reprinted from Sehnal 1239, Copyright © 1985, page 65, with permission from Elsevier Science Ltd, The Boulevard, Langford Lane, Kidlington OX5 1GB, UK
Figure 22. Figure 22.

Percentage conversion of androstendione (δ4), progesterone (P4), and dehydroepiandrost‐erone (DHEA) in 1 h by 0.1 g of ovary and testes tissue of Asterias rubens at different times of the year. Stage values refer to index of Schoenmakers et al. 1213; oocytic diameters increase from 1 to 4, with spawning during late 4 and early 1.

From Voogt et al. 1416, reprinted with permission
Figure 23. Figure 23.

Immunocytohistological methods were used to identify FMRFamide immunoreactivity in the cerebral ganglia (gc) of the helminth Echinosoma liei. Scale bar‐100 μm.

From Riddell et al. 1137, reprinted with permission
Figure 24. Figure 24.

Bombyxin, an insect peptide, is related to synthesis of ecdysone. Distribution of neurosecretory cells immunoreactive to the monoclonal antibombyxin antibody in brains of adults of Eisenia fetida. 1: Transverse section through the right part of the brain (B) and the circumpharyngeal connective (Cp), showing one immunoreactive cell (arrow). Ph, pharynx. Bar = 120 μm. 2: Frontal section of brain showing two immunoreactive cells (arrows) symmetrically localized in lateral areas. Bar = 120 μm. 3: Immunoreactive material in a neurosecretory cell (Nc) and its axon (arrows). Bv: blood vessels. Bar = 15 μm.

From Sauber et al. 1198, reprinted with permission
Figure 25. Figure 25.

Structures of the pheromone components of the housefly Musca domestica.

From Blomquist et al. 105, reprinted with permission of Academic Press, Inc
Figure 26. Figure 26.

Chemical synthesis of bombykal (1).

From Bestmann et al. 80. Reprinted with permission of Birkhauser Verlag AG
Figure 27. Figure 27.

I, II: Dihyropyrrolizine pheromones of arctiid moths; III, IV: gas‐liquid cheomatographic degradation products of II.

From Krasnoff et al. 759, with permission of Plenum Publishing Corp
Figure 28. Figure 28.

Structures of sex pheromone components produced by female Periplaneta americana. Left to right: periplanone B, Persoons' periplanone‐A, Hauptmann's periplanone‐A.

From Okada et al. 996, reprinted with permission of Plenum Publishing Corp
Figure 29. Figure 29.

Sterochemical structures (A) and stereospecific bioactivity (B) of 4‐methyl‐3‐heptanol.

From Steghaus‐Kovac et al. 1314, reprinted with permission of Birkhäuser Verlag AG
Figure 30. Figure 30.

Alarm response to a strong stimulus (A) immediately before first overt response; (B) 0.3 s later, after the first of three rapid tentacle flexures; (C) 1 s after B, contraction of the mesenterial retractors; (D) 1.5 s after C, constriction of the marginal sphincter.

From Howe and Sheikh 605, reprinted with permission. Copyright © 1975 by the American Association for the Advancement of Science


Figure 1.

Chemical structures of ecdysteroids.

From Sakurai and Gilbert 1189, reprinted with permission of Springer‐Verlag, Inc


Figure 2.

Chemical structures of JH‐like compounds.

From Laufer and Biggers 796, reprinted with permission of Peeters Press, Inc


Figure 3.

Blood hormone titers during metamorphosis in Manduca. Time in days. IV‐L, fourth larval instar; V‐L, fifth larval instar; P, pupa; DA, developing adult; A, adult; E, ecdysis (the shedding of the old cuticle); CP, commitment pulse; PP, prepupal peak. Hormone titers are from Bollenbacher et al. 122 and Riddiford 1138. Peak blood ecysteroid titers during the commitment pulse and prepupal peak are (in 20E equivalents) 0.07 and 1.5 μg/ml, respectively, and the maximum value during adult development is 3 μg/g fresh weight 122.

From Weeks and Truman 1442. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc


Figure 4.

Schematic diagram illustrating the control of molting and metamorphosis in the tobacco hornworm moth.

From Gilbert 466 and Gilbert and Goodman 467, reprinted with permission of Sinaver Associates, Inc


Figure 5.

JH titer in the hemolymph of adult female Leptinotarsa decemlineata reared under different photoperiods. Upper graph: GU, Galleria units, after de Wilde et al. 307. Lower graph: measured by gas chromatography/mass spectrometry. LD, long day; SD, short day.

From de Wilde 305. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc


Figure 6.

Extirpated Y‐organ of Orconectes limosus; c, thin cutile, separating the Y‐organ from the branchial chamber; arrow: basement membrane of individual lobule; bs, blood sinus. Azan stain, paraffin section.

From Keller and Willig 709, reprinted with permission of Springer‐Verlag and R. Keller


Figure 7.

Major endocrine and neuroendocrine structures of generalized female Crustacea. Included are the organs important for female reproduction, the eyestalk, sinus gland X‐organ, the mandibular organ, Y‐organ, and thoracic ganglion.

From Laufer et al. 802


Figure 8.

Control (c) stages III and IV, and eyestalkless (es–) stages IVa, IV', and IV that result from eyestalk ablation in stage II.

From Charmantier et al. 197, reprinted with permission


Figure 9.

Radiochromatogram on HPLC system 2(a) of an aliquot of the 100% methanolic silicic acid column fraction from Nereis diversicolor after injection of [3H]ecdysone and maintenance for 24 h. Fractions were collected every 30 s for scintillation counting. The positions of authentic ecdysone (I), 20‐hydroxyecdysone (II), 20‐hydroxyecdysone‐22‐phosphate (V), 20‐hydroxyecdysone acid (VI), ecdysone‐22‐phosphate (VII), and ecdysonic acid (VIII) are shown.

From Mercer et al. 914, reprinted with permission


Figure 10.

Example of simple tissue repair. Penaeus monodon female showing completely healed right eye after ablation; left eye has been tagged for rematuration experiments.

From Primavera 1078, reprinted with permission


Figure 11.

Distribution of ganglion cells (circles) and epidermal sensory cells (triangles) in the tentacles and hypostome. One tentacle is shown in full, while others have been truncated.

From Bode et al. 108, reprinted with permission of American Zoologist


Figure 12.

Experiment illustrating the conversion of FLI‐ to FLI + neurons during head regeneration. Circles and triangles represent FLI+ ganglion and FLI+ epidermal sensory cells, respectively. HU, hydroxyurea; NM, nitrogen mustard; FLI, FMR Famide‐like immunoreactivity.

From Bode et al. 108, reprinted with permission of American Zoologist


Figure 13.

Platynereis dumerilii, posterior regenerates. Photomicrographs of live specimens a: Typical caudal regenerate grown under the hormonal control of an intact prostomium. The endocrine status of prostomia of experimental animals which exhibited this type of regenerate was designated “active.” b: Atypical posterior regenerate developed under nonhormonal conditions. The endocrine status of prostomia of experimental animals exhibiting this type of regenerate and showing epitokoid development was designated “inactive.” Note rudimentary parapodium (arrow) and digitiform outgrowths of the pygidium, typical for the epitokous males, which evacuate sperm. 1, Parapodium of former wound segment; 2, regenerated pygidium; 3, urite (appendage of pygidium); 4, parapodium of regenerated segment.

From Hofmann 577,578, reprinted with permission


Figure 14.

Regeneration in snails with one cerebral ganglion removed was evaluated upon death 2 to more than 24 months after the lesion. Results were arbitrarily grouped into four time periods. The state of repair was categorized as no communication through the side of the missing ganglion (N), tract stage (T), bud stage (B), or ganglion stage (G). Distribution within these four categories was plotted as percent of the total number (n) of animals examined in each postoperative time period.

From Moffet and Ridgway 926. Reprinted with permission of American Zoologist


Figure 15.

The eyestalk of Palaemon serratus showing sites immunopositive for antiadipokinetic hormone sera, which can be used to detect red pigment–concentrating hormone.

From Bellon‐Humbert et al. 57, reprinted with permission of Biological Bulletin, LG, lamina ganglionaris; ME, medulla externa; MI, medulla interna; MT, medulla terminalis; MEX, medulla externa of X‐organ; MTGX‐1 and −2, medulla terminalis of X‐organs 1 and 2; OB, organ of Bellonci; SG, sinus glands; +, neurosecretory cells


Figure 16.

Diagrammatic composite decapod crustacean illustrating neuroendocrine centers (1, eyestalk system; 2, brain; 3, thoracic ganglion; 4, pericardial organ) and osmoregulatory sites (5, stomach; 6, intestine; 7, gill; 8, antennal gland; 9, intracellular).

From Kamemoto 678, reprinted with permission of American Zoologist


Figure 17.

Methyl farnesoate (MF) synthesis varies with embryonic development, which itself reflects ovarian growth.

From Laufer et al. 799, reprinted with permission. Copyright © 1987 by the American Association for the Advancement of Science


Figure 18.

Histological section of androgenic gland implant recovered from masculinized female. Arrows, androgenic gland; v, muscle of vas deferens. Bar = 100 μm. Androgenic glands from Procambrus males recovered after transplantation into females for 326 days.

From Nagamine and Knight 961, reprinted with permission


Figure 19.

Diagrammatic representation of the composite effects of JH in species whose vitellogenesis depends on JH‐controlled vitellogenin synthesis.

From Engelmann 363,364. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc


Figure 20.

Model for control of egg development in Aedes aegypti. EDNH, egg development neurosecretory hormone.

From Hagedorn 517. Copyright © 1983, A. R. Liss, Inc. Reprinted by permission of Wiley‐Liss, a division of John Wiley and Sons, Inc


Figure 21.

Alternative reproductive cycles of Heteropeza pygmaea (Diptera, Cecidomyiidae). Larva (L) derived from the egg (E) develops into pedogenetic female “mother larva” (M♀) producing undetermined daughter larvae (TL). Each daughter larva may become either a female mother larva, a female “imago‐larva” (IL♀), a male mother larva (M♂), and/or a mother larva with mixed progeny (M♀♂). P, pupa; I, imago.

From Weber 1436 and Sehnal 1239. Reprinted from Sehnal 1239, Copyright © 1985, page 65, with permission from Elsevier Science Ltd, The Boulevard, Langford Lane, Kidlington OX5 1GB, UK


Figure 22.

Percentage conversion of androstendione (δ4), progesterone (P4), and dehydroepiandrost‐erone (DHEA) in 1 h by 0.1 g of ovary and testes tissue of Asterias rubens at different times of the year. Stage values refer to index of Schoenmakers et al. 1213; oocytic diameters increase from 1 to 4, with spawning during late 4 and early 1.

From Voogt et al. 1416, reprinted with permission


Figure 23.

Immunocytohistological methods were used to identify FMRFamide immunoreactivity in the cerebral ganglia (gc) of the helminth Echinosoma liei. Scale bar‐100 μm.

From Riddell et al. 1137, reprinted with permission


Figure 24.

Bombyxin, an insect peptide, is related to synthesis of ecdysone. Distribution of neurosecretory cells immunoreactive to the monoclonal antibombyxin antibody in brains of adults of Eisenia fetida. 1: Transverse section through the right part of the brain (B) and the circumpharyngeal connective (Cp), showing one immunoreactive cell (arrow). Ph, pharynx. Bar = 120 μm. 2: Frontal section of brain showing two immunoreactive cells (arrows) symmetrically localized in lateral areas. Bar = 120 μm. 3: Immunoreactive material in a neurosecretory cell (Nc) and its axon (arrows). Bv: blood vessels. Bar = 15 μm.

From Sauber et al. 1198, reprinted with permission


Figure 25.

Structures of the pheromone components of the housefly Musca domestica.

From Blomquist et al. 105, reprinted with permission of Academic Press, Inc


Figure 26.

Chemical synthesis of bombykal (1).

From Bestmann et al. 80. Reprinted with permission of Birkhauser Verlag AG


Figure 27.

I, II: Dihyropyrrolizine pheromones of arctiid moths; III, IV: gas‐liquid cheomatographic degradation products of II.

From Krasnoff et al. 759, with permission of Plenum Publishing Corp


Figure 28.

Structures of sex pheromone components produced by female Periplaneta americana. Left to right: periplanone B, Persoons' periplanone‐A, Hauptmann's periplanone‐A.

From Okada et al. 996, reprinted with permission of Plenum Publishing Corp


Figure 29.

Sterochemical structures (A) and stereospecific bioactivity (B) of 4‐methyl‐3‐heptanol.

From Steghaus‐Kovac et al. 1314, reprinted with permission of Birkhäuser Verlag AG


Figure 30.

Alarm response to a strong stimulus (A) immediately before first overt response; (B) 0.3 s later, after the first of three rapid tentacle flexures; (C) 1 s after B, contraction of the mesenterial retractors; (D) 1.5 s after C, constriction of the marginal sphincter.

From Howe and Sheikh 605, reprinted with permission. Copyright © 1975 by the American Association for the Advancement of Science
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Article Title: Invertebrate Endocrinology
 

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Matthew Landau, William J. Biggers, Hans Laufer. Invertebrate Endocrinology. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1291-1390. First published in print 1997. doi: 10.1002/cphy.cp130218