Eur. J. Entomol. 107 (1): 13-31, 2010 | 10.14411/eje.2010.002

Physiology of heartbeat reversal in adult Drosophila melanogaster (Diptera: Drosophilidae)

Karel SLÁMA
Institute of Entomology, Biological Centre of Czech Academy of Sciences, Drnovská 507, 161 00 Praha 6, Czech Republic;

Heartbeat patterns were monitored in the living bodies of decapitated adult flies using several electrocardiographic methods (pulse-light optocardiography, thermocardiography, strain-gauge cardiography). Unlike other insect species, in which there is a peristaltic segmental propagation of cardiac contractions, Drosophila uses extremely efficient synchronic cardiac contractions. The rate of synchronic cardiac pulsation, which is characterized by simultaneous propagation of anterograde systolic contractions along all the segments of the heart, is relatively fast (~ 4 Hz at room temperature). This pulsation is used mainly for the vigorous pumping of haemolymph into the head and thorax through a narrow elastic tube, the aorta (anterograde I heartbeat). In addition, this synchronic pulsation is also used to enhance the circulation of haemolymph throughout the abdominal body cavity (anterograde II heartbeat). The switch between thoracic (anterograde I) and abdominal (anterograde II) haemolymph circulation is regulated by periodically alternating, tetanic contractions and relaxations of the conical heart chamber (ventricle). In the latter there is a pair of slit-like apertures, which are closed or opened by contraction or relaxation of the organ, respectively. During contraction of the conical chamber, the apertures are tightly constricted for several seconds and haemolymph is pumped forwards into the aorta (anterograde I heartbeat). Conversely, during relaxation of the conical chamber, the apertures are wide open for a few seconds, haemolymph leaves the heart and leaks out through open apertures and circulates from the tail to the base of the abdomen. The backward oriented, retrograde heartbeat recorded in other insects, has a lower frequency (1 to 2 Hz), occurs in Drosophila only sporadically and usually in the form of individual or twinned systolic peaks of large amplitude. Unlike the synchronic nature of the anterograde I and II cardiac contractions, propagation of the relatively slow retrograde heartbeat is by peristalsis. The newly discovered, compact ventricle with atrium and synchronic functioning of the insect heart shows structural and functional analogies with the functioning of the human heart.

Keywords: Peristaltic heartbeat, synchronic heartbeat, pulse-light optocardiography, thermocardiography, strain-gauge cardiography

Received: March 9, 2009; Accepted: June 17, 2009; Published: February 15, 2010

Download citation

References

  1. AI H. & KUWASAWA K. 1995: Neural pathways for cardiac reflexes triggered by external mechanical stimuli in larvae of Bombyx mori. J. Insect Physiol. 41: 1119 -1131 Go to original source...
  2. AKASAKA T., KLINEDIENST S., OCCOR K., BUSTAMANTE E.L., KIM S.K. & BODMER R. 2006: The ATP-sensitive potassium (KATP) channel-encoded dSUR gene is required for Drosophila heart function and is regulated by tinman. PNAS 103: 11999-12004 Go to original source...
  3. BODMER R. 1995: Heart development in Drosophila and its relationship to vertebrate systems. Trends Cardiovasc. Med. 5: 21-27 Go to original source...
  4. BODMER R. & VENKATESH T.V. 1998: Heart development in Drosophila and vertebrates: conservation of molecular mechanisms. Devel. Genet. 22: 181-186 Go to original source...
  5. BODMER R., WESSELLS R.J., JOHNSON E.C. & DOWSE H.B. 2005: Heart development and function. In Gilbert L.I., Iatrou K. & Gill S. (eds): Comprehensive Molecular Insect Science. Vol 2. Elsevier, Oxford, pp. 199-250
  6. COATS J.R. 1982: Insecticide Mode of Action. Academic Press, New York, London, 470 pp
  7. CURTIS N.J., RINGO J.M. & DOWSE H.B. 1999: Morphology of the pupal heart, adult heart and associated tissues in the fruit fly, Drosophila melanogaster. J. Morphol. 240: 225-235 Go to original source...
  8. DULCIS D. & LEVINE R.B. 2005: Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster. J. Neurosci. 25: 271-280 Go to original source...
  9. DULCIS D., DAVIS N.T. & HILDEBRAND J.G. 2001: Neuronal control of heart reversal in the hawkmoth Manduca sexta. J. Comp. Physiol. (A) 187: 837-849 Go to original source...
  10. JONES J.C. 1977: The Circulatory System of Insects. Charles C. Thomas, Springfield, 33 pp
  11. KLOWDEN M.J. 2007: Physiological Systems in Insects. 2nd ed. Elsevier, Oxford, 688 pp
  12. KRIJGSMAN B.J. 1952: Contractile and pacemaker mechanisms of the heart of arthropods. Biol. Rev. 27: 320-346 Go to original source...
  13. MILLER T.A. 1979: Nervous versus neurohormonal control of insect heartbeat. Am. Zool. 9: 77-86. Go to original source...
  14. MILLER T.A. 1985: Structure and physiology of the circulatory system. Comp. Insect Physiol. Biochem. Pharmacol. 3: 289-353
  15. MILLER T.A. 1997: Control of circulation in insects. Gen. Pharmacol. 29: 23-38 Go to original source...
  16. NATION J.L. 2002: Insect Physiology and Biochemistry. CRC Press, Boca Raton, 485 pp
  17. NICHOLS R., KAMINSKI S., WALLING E. & ZORNIK E. 1999: Regulating the activity of a cardioacceleratory peptide. Peptides 20: 1153-1158 Go to original source...
  18. OCORR K., PERRIN L., LIM H.-Y., QIAN L., WU X. & BODMER R. 2007: Genetic control of heart function and aging in Drosophila. Trends Cardiovasc. Med. 17: 177-182 Go to original source...
  19. RICHTER K. 1973: Struktur und Funktion der Herzen wirbelloser Tiere. Zool. Jb. Physiol. 77: 477-668
  20. RIZKI T.M. 1978: The circulatory system and associated cells and tissues. In Ashburner M. & Wright T. (eds): The Genetics and Biology of Drosophila. Vol. 2a. Academic Press, New York, pp. 397-452
  21. SLAMA K. 2000: Extracardiac versus cardiac haemocoelic pulsations in pupae of the mealworm (Tenebrio molitor L.). J. Insect Physiol. 46: 977-992 Go to original source...
  22. SLAMA K. 2003: Mechanical aspects of heartbeat reversal in pupae of Manduca sexta. J. Insect Physiol. 49: 645-657 Go to original source...
  23. SLAMA K. 2004: The effect of Corazonin on heartbeat reversal in pupae of the tobacco hornworm, Manduca sexta. Eur. J. Entomol. 101: 513-521 Go to original source...
  24. SLAMA K. 2005: Neuropeptides and insect heartbeat: the myth and reality. Pestycydy (Pesticides) 3: 95-107
  25. SLAMA K. 2006: Heartbeat reversal after sectioning of the dorsal vessel and removal of the brain in diapausing pupae of Manduca sexta (Lepidoptera: Sphingidae). Eur. J. Entomol. 103: 17-26 Go to original source...
  26. SLAMA K. 2008: Extracardiac haemocoelic pulsations and the autonomic neuroendocrine system (coelopulse) of terrestrial insects. Terrest. Arthrop. Rev. 1: 39-80 Go to original source...
  27. SLAMA K. & FARKAS R. 2005: Heartbeat patterns during the postembryonic development of Drosophila melanogaster. J. Insect Physiol. 51: 489-503 Go to original source...
  28. SLAMA K. & MILLER T.A. 2001: Physiology of heartbeat reversal in diapausing pupae of the tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae). Eur. J. Entomol. 98: 415-431 Go to original source...
  29. SLAMA K. & ROSINSKI G. 2004: Pharmacological effects of proctolin and CCAP on heartbeat in pupae of the tobacco hornworm, Manduca sexta. Physiol. Entomol. 30: 14-28 Go to original source...
  30. SLAMA K., SAKAI T. & TAKEDA M. 2006: Effect of corazonin and CCAP on heartbeat in the adult American cockroach (Periplaneta americana). Arch. Insect Biochem. Physiol. 62: 91-103 Go to original source...
  31. TOGEL M. & PASS G. 2006: Funktionsmorphologische und phylogenetische Aspekte der Herzschlagumkehr bei Insekten. Entomol. Austr. 13: 39-46
  32. TUBLITZ N. 1989: Insect cardioactive peptides: Neurohormonal regulation of cardiac activity by two cardioacceleratory peptides during flight in the tobacco hawkmoth, Manduca sexta. J. Exp. Biol. 142: 31-48
  33. TUBLITZ N. & TRUMAN J.W. 1985: Insect cardioactive peptides. II. Neurohormonal control of heart activity by two cardioacceleratory peptides in the tobacco hawkmoth, Manduca sexta. J. Exp. Biol. 114: 381-395
  34. VEENSTRA J.A. 1989: Isolation and structure of corazonin, a cardioactive peptide from American cockroach. FEBS Letters 250: 231-234 Go to original source...
  35. WASSERTHAL L.T. 1996: Interaction of circulation and tracheal ventilation in holometabolous insects. Adv. Insect Physiol. 6: 297-351 Go to original source...
  36. WASSERTHAL L.T. 1999: Functional morphology of the heart and of a new cephalic pulsatile organ in the blowfly Calliphora vicina (Diptera: Calliphoridae) and their roles in hemolymph transport and tracheal ventilation. Insect Morph. Embryol. 28: 111-129 Go to original source...
  37. WASSERTHAL L.T. 2007: Drosophila flies combine periodic heartbeat reversal with a circulation in the anterior body mediated by a newly discovered anterior pair of ostial valves and 'venous' channels. J. Exp. Biol. 210: 3707-3719 Go to original source...
  38. WIGGLESWORTH V.B. 1965: The Princioples of Insect Physiology. 6th ed. Methuen, London, New York, 741 pp
  39. ZEITOUNI B., SENATORE S., SEVERAC D., AKNIN C., SEMERIVA M. & PERRIN L. 2007: Signalling pathways involved in adult heart formation revealed by gene expression profiling in Drosophila. PLoS Genetics 3: 1907-1921 Go to original source...
  40. ZORNIK E., PAISLEY K. & NICHOLS R. 1999: Neural transmitters and a peptide modulate Drosophila heart rate. Peptides 20: 45-51 Go to original source...