Though Drosophila melanogaster has been poked and prodded for decades as a model organism in numerous lines of research, a new study published in the Journal of Experimental Biology has identified new anatomy in the fruit fly's heart. The findings help explain a phenomenon in which the direction of their heartbeat reverses, the study's author says.
"In some sense it's like finding a third eye, at least in the world of circulation," Tom Miller, an entomologist at the University of California, Riverside, told The Scientist. "Particularly in Drosophila melanogaster, when we're supposed to know more about it than most other animals."
Scientists have observed heartbeat reversals in a number of different insects, including fruit flies, and it is thought to help improve the flow of hemolymph (the blood of the insect, which does not carry oxygen) throughout the body.
Lutz Wasserthal from the University of Erlangen-Neurnberg took a closer look at the behavior and recorded heart movements from D. melanogaster and D. hydei using an infrared beam shone through the body, with a recording sensor on the other side. Animals' heartbeats alternated between forward (anterograde) and backward (retrograde) periods.
In addition to describing the reversals, Wasserthal used light and electron microscopy to find what anatomy might be responsible for the behavior. He identified a fifth pair of ostia -- openings in the heart that allow the flow of hemolymph. In Drosophila, the four known pairs of ostia are responsible for hemolymph intake during regular heartbeats that direct flow from the abdomen toward the head of the animal.
Wasserthal proposes that this new pair of ostia, which are located anterior to the others, take in hemolymph from the thorax and move it posteriorly toward the abdomen. He found that the ostia connect to previously-undescribed hemolymph channels in the thorax and he also discovered an opening at the caudal end of the heart.
Harold Dowse at the University of Maine told The Scientist that Wasserthal's technique for recording the heartbeats is an important step forward to advancing fly heart research. "I've seen figures like that for much larger insects, but to get that kind of a picture of reversal in the fly is really nice," Dowse said.
The newfound anatomy "enlarges our understanding of how the thorax is involved in circulating the hemolymph," Rolf Bodmer at the Burnham Institute for Medical Research told The Scientist.
"Without the knowledge of the anterior and posterior openings the blood flow by regular heartbeat reversals would not be understandable," Wasserthal wrote in an Email to The Scientist. He expected to find the structures in the fruit fly because he also uncovered them in the blow-fly eight years ago.
Wasserthal wrote that the structures in the heart went overlooked because the anatomy is buried under a muscular sheath and fat body, making them invisible during ventral dissections. Additionally, they are delicate and tend to get damaged easily during dissection.
The findings support Wasserthal's theory as to why fruit flies periodically reverse the direction of hemolymph movement -- that it helps them actively take in more air. "All people thought until now that Drosophila doesn't ventilate," Wasserthal said in an interview. Larger insects actively ventilate air by expanding and contracting their trachea. It was assumed that because the fruit fly is small and its hemolymph does not carry oxygen that its respiratory system operated by passive diffusion like other small insects. But Wasserthal said the animals also ventilate by heartbeat reversal.
He explained that during backward heartbeats, hemolymph volume in the head and thorax decrease, which is compensated by an inflation of the air sac, making the animal inspire during backward beats and expire during forward heartbeats. "Thus in Drosophila tracheal ventilation is performed by hemolymph shift as in the larger insects," Wasserthal wrote.
Dowse agreed that "anatomically at this point it's a possibility. But he needs to make the case physiologically." Miller concurred, noting, "this all makes perfect sense to me," but it needs to be corroborated by other labs. A next step would be to monitor how the hemolymph flows during the heartbeat, said Bodmer.
Miller says Wasserthal's anatomical discoveries speak to the value of old techniques like morphology, and of well-worn models. "Insects are still a rich goldmine for finding things to study."
By Kerry Grens
mail@the-scientist.com
Links within this article:
R. Lewis, "Flies invade human genetics," The Scientist, June 22, 1998.
http://www.the-scientist.com/article/display/18086/
Wasserthal L.T., "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, 210:3709-19, 2007.
http://jeb.biologists.org/cgi/content/abstract/210/21/3707
Tom Miller
http://www.faculty.ucr.edu/˜chmeliar/miller_home/home.htmlWasserthal L.T., "Flight-motor-driven respiratory air flow in the hawkmoth Manduca sexta," J Exp Biol, 204:2209-20, 2003.
http://www.the-scientist.com/pubmed/11507105
Harold Dowse
http://biology.umaine.edu/run.php?pg=User&user_id=65
Rolf Bodmer
http://www.burnham.org/default.asp?contentID=133
Wasserthal L.T, "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," Int J Insect Morphol Embryol, 128:111-29. 1999.
http://tinyurl.com/2hay6d
T. Toma, "Breathing bugs," The Scientist, January 24, 2003.
http://www.the-scientist.com/article/display/21044/

[Comment posted 2007-11-18 12:17:08]
Both beautiful publications mentioned by Laurent Perrin would have needed to be considered in my paper, but as a non-developmental biologist I was not acquainted with the two recent publications in the field of heart gene activation. The aspect of the described first ostia was not traceable by electronic key word search.
I have meanwhile read the publication of Monier et al. 2005 (Perrin's lab). The paper gives a complete schematic sketch of the adult Drosophila heart with 5 pairs of ostial valves. This drawing is based on the convincing documentation of 5 pairs of ANLAGEN in the course of heart metamorphosis, best visible in the Fig. 2, 30 hours after puparium formation. In the supplemental Fig. 2C of an isolated heart of the adult, they point at the position of the first ostia (arrowhead) but the structure of the adult ostia is not really visible.
The paper of Monier et al. 2005 does not make any point about the fact, that a 5th pair of ostial valves in A1 would mean one pair more than hitherto known in adult Drosophila. A "new" additional pair of ostial valves is not discussed and not mentioned in the abstract.
In a comparable analysis, the Paulutat group (Sellins et al. 2006) deals with the metamorphosing heart and point in Fig. 8F not to the first ostia but only to the (luminal) valve building cells in A1. They do not discuss the number of adult ostia in Drosophila, which are not documented as fully developed structures. Also in this paper neither title nor abstracts or key words contain hints to the new or additional first ostia and the difference from the hitherto known anatomical situation in adult Drosophila.
Under a genetic point of view, without knowing the central function, the impact of the occurrence of these first ostia seems not to have been of special interest.
It is a general problem to have a complete actual overview of both genetic and morphologic fields of investigation. The researchers of the Drosophila heart also overlooked more recent papers about the calliphorid heart (Angioy et al.1999; Wasserthal, L. T. (1999) containing not only the complete set of ostia but also a well documented caudal heart opening not yet addressed in developmental research, although heart anatomy in these flies is almost identical.
The publications of Monier et al. 2005 and Sellins et al. 2006 provide already the developmental complementation postulated in my paper on heart function.
Angioy, A.M., Boassa, D. and Dulcis, D. (1999). Functional morphology of the dorsal vessel in the adult fly Protophormia terraenovae (Diptera, Calliphoridae). J. Morphol. 240, 15-31;
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. Arthropod Structure & Development 28 (1-2) (1999) pp. 111-129.
[Comment posted 2007-11-06 11:35:03]
In addition, we recently reported an analysis of the formation of the adult heart by whole genome transcriptome dynamic analysis, which allowed us to point out that the Wnt pathway is involved in ostias formation, while the PVR (PDGF-VEGF) signalling pathway is required for the formation of 3 pairs of valves which separate the tube into a 4 chambered heart in the adult. Zeitouni B, S←natore S, S←verac D, Aknin C, S←m←riva S and Perrin L. Signalling pathways involved in cardiogenesis revealed by gene expression profiling in Drosophila. PLoS Genet. 2007 Oct 12;3(10)
[Comment posted 2007-10-25 12:23:21]
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