Scouring the literature on Drosophila reproduction for my research, I’ve encountered  illustrations of the fruit fly female reproductive tract (FRT) that range from intricate and realistic to simple line drawings. I started paying attention to these different styles when I was working on my own figure for a recent review paper. I went through several iterations of sketches before creating one that felt accurate in my drawing style (top). My co-authors and I then worked with a designer who digitized my drawing, added shading, and provided us with an image we could annotate with changes (middle). We then had long discussions about how to improve the distribution of cells surrounding the spermatheca (ST), the shape and placement of the seminal receptacle (SR) and how to make the cortical appendages of the egg look less ‘spiky’. In the end, we created a figure that has a simplified cartoon aesthetic that I think is accurate and easy to understand (bottom). During this process, I amassed a collection of 28 different representations of the D. melanogaster FRT, and became increasingly curious about which styles predominate and whether they change over time or based on research focus. I found that most illustrations of the FRT tend to emulate one of the three earliest depictions (ours is a combination of the Patterson and Miller styles – see below), but that even figures by the same person or research group can be vastly different. I also saw that FRT figures in research related to neurological systems or development tend to have a distinguishable style. The enormous variation in depictions of the FRT highlights how the perspective of a scientist can influence the visualization of a subject.

The first drawing of the Drosophila FRT, that I have found, is from 1920 by J. F. Nonidez. Following unsuccessful attempts at artificial fertilization Nonidez, with guidance from T.H. Morgan, published a detailed description of reproductive structures and postcopulatory processes. His drawing has a very textured exterior, an uncoiled SR, and an ovary that accentuates eggs at various stages of maturation. However, Nonidez’s representation is rather obscure and rarely republished. The FRT drawings by J.T. Patterson (1943) and A. Miller (1950) are much more iconic, and the influence of their artistic styles can be seen in many of the current depictions. Patterson was an incredible naturalist who drew the FRT of over 50 species (all available on FlyBase), and the popularity of his drawings is likely a result of his ability to capture the feel of the structure in a realistic style that is also simple. In contrast, Miller’s line drawing forgoes the 3 dimensionality of his predecessors and instead incorporates additional details, such as fat bodies surrounding the ST, musculature, and isolated ovarioles. His FRT is part of a text on anatomy and histology, and the difference in style is likely a result of a research direction increasingly focused on mechanisms, development, and molecular biology.

Although the most common representation of the FRT is from a ventral perspective (seminal receptacle facing the front) and stretched/ flattened so the ovaries form a “Y” shape, both Nonidez (1920) and Miller (1950) also included the FRT from a parasagittal perspective. This view shows the FRT from the side, and is a more accurate depiction of the spatial distribution of the sperm storage organs (ST and SR). Nonidez’s cross section excludes the ovaries, but shows an egg within in the bursa and the secretory cells surrounding the lumen of the parovaria (PO) and ST. A simplified version of this drawing was replicated in K.G. Davey’s 1985 review of insect female reproductive tract structure and function. Miller’s parasagittal view shows the FRT situated within the abdomen of the female. This image most accurately represents the in vivo curvature of the oviduct, and the physical connections between the ST, PO, and the rectum. A version of this figure with added colors, nerves, and arrows is in R.I. Bailey et al.’s 2011 paper on gene expression changes and mate choice. The only other depiction of the paragsagital FRT within the female abdomen is in V. Hartenstein’s 1993 Atlas of Drosophila Development (available on sdbonline.org). This figure shares many similarities with Miller, except the the shape of the structures, particularly the ovary and PO, are more stylized.

Many of the modern FRT illustrations can be found in the research and review papers of M.F. Wolfner and her lab. Wolfner is an eminent scientist in the area of Drosophila  reproduction, and her research has uncovered, in incredible detail, the effects and mechanisms of seminal fluid proteins on female postmating response. The drawings of the FRT in her research are also amazing because they include so many different interpretations, and usually explicitly acknowledge the artist. Earlier figures from 1997, 1999, and 2002 are highly simplified, they forgo accuracy of structure shape, position, and presence, to create a generalized image of the FRT. This type of figure can be useful because it highlights only the parts of a complex system that are relevant to the research discussed. The 1999 figure appears to be a modified outline of Miller’s 1950 illustration, while the 1997 (by S. Monsma, shown here from a reprint in 2005) and 2002 illustrations look to be line drawings that may be computer generated. In addition, the FRT illustration from a 2013 research paper on ovulin signaling shares a resemblance to the 2002 drawing, with additional shading, a more detailed SR (coiled in the Patterson style), and different ovaries. In 2009, 2011 and 2015 Wolfner’s graduate student J.L. Sitnick drew three different representations of the FRT. Although these drawings are all by the same artist, they are delightfully different. The position of the FRT, shading style, and coiling of the SR vary between the drawings. In addition, the ovaries are very distinct, with many developing eggs visible in the 2009 figure while only mature eggs are easily visible in the 2011 figure. My favorite drawing is by A. Yori in a 2007 paper on morphological changes in the FRT postmating. These drawings show details such as genital hairs and oviduct/bursa conformation in a way that few others attempt. They are hyper-realistic and have a complexity to them that feels more accurate, although it can be harder to understand.

Research on postmating changes to the FRT by other groups have also included their own FRT illustrations. The FRT drawing in Mack et al. 2006 highlighted the section of “lower FRT” they used for a study of gene expression changes postmating. This image is similar Miller’s line drawing, except it is a parasagital view, the ovaries are much squatter and the SR is coiled and rather small. Kapelnikov et al. 2008 included a very stylized computer graphic illustration  based on the Patterson drawing. The simplified, easy to understand, image effectively delineates the major sections of the FRT. Versions of this figure have appeared in several articles and shown here is the updated color-coded and labeled figure from I. Carmel et al. 2016. The FRT illustration in S.L. Schanakenberg et al.’s 2012 review of sperm storage is more complex, and bares a slight resemblance to Nonidez’s drawing. This depiction is the only one to use dark space in the ovary, has clearly defined secretory cells that are distributed only around parts of the SST and includes genital hairs.

Figures associated with research focused on neurobiology can often be distinguished by the brightly colored neurons innervating the FRT. H. Hertweck’s 1931 drawing is a funny cartoon-like depiction of the FRT, without the ovaries, in its contorted in vivo conformation. This drawing looks nothing like the current neurobiology representations of the FRT, except for the prominent presence of a neuron. The drawing in Middleton et al. 2006 is highly reminiscent of Miller, except without isolated ovarioles and from a dorsal perspective so that the SR is face down and not visible. The lower half of Hasemeyer et al.’s 2009 FRT figure is also Miller-esque, while the ovaries look more like Nonidez’s drawing. The ovaries are different from other depictions they are enclosed in a peritoneal sheath. Although he Feng et al. 2014 figure is from the same research group as the Hasemeyer figure, it has a very different appearance. The Feng et al. FRT is situated within the abdomen, has much heavier computer generated shading, and the SR is larger and coiled.

The final category is FRT figures from developmental biology research. These figures also have a distinct style, they tend to exclude the ovaries, use the parisagital perspective, and preferentially include structures that arise from the genital imaginal disc, including the FRT, external genitalia,and analia. P.J. Bryant’s illustration of the FRT in 1978  is very clear, with light shading, a coiled SR, long oviduct, and visible secretory cells in the ST and PO. Bryant’s illustration frequently appears in recent development papers as the image of the mature FRT. The drawing in Chen et al. 1997 has an oviduct and SR similar to Bryant, but is drawn from a different angle with a greater focus on the external genitalia. The bursa of this illustration is also more shaded and textured in a style evocative of Nonidez.  Estrada et al. 2003 also included their own figure that looks like a simplified fusion of both the Bryant and Chen et al. drawings. The color coding is a useful addition and denotes the the parts of the FRT that arise from different segments of the genital disc. The FRT from Epper 1983 is technically from the late pupal stage and not an adult. However, the flat and almost child-like drawing, that is also very detailed, has a strange, joyful, quality to it that I could not resist.

What does the female reproductive tract of the fruit fly look like? It turns out the question is not nearly as easy to answer as I thought it would be. Even pictures of the FRT from microscopy can look different depending on the dissection, the type of microscope, the angle, and the focus. In drawings, there are additional confounding factors such as style and extent of detail. I love how variable and personal drawings of the FRT can be, they demonstrate how the appearance of a structure can be shaped by the focus and interests of the artist and/or scientist. Scientists have continued to create drawings and figures of the FRT over the past century, because they are valuable in tool in communicating research.

Let me know if I missed any FRT figures, or if you have a favorite!

Citations

Fig.1 My Figure

2016 – C.E. McDonough, E. Whittington, S. Pitnick, S. Dorus, Proteomics of reproductive systems: insights into the molecular basis of postmating-prezygotic reproductive barriers.

Fig. 2 Early Ventral Figures

1920 – J.F. Nonidez, The Internal Phenomena of Reproduction in Drosophila

1943 – J.T. Patterson, The Drosophila of the Southwest

1950 – A. Miller, The Internal Anatomy and Histology of the Imago of Drosophila Melanogaster

Fig. 3 Early Parasagital Figures

1920 Nonidez & 1950 Miller, see above

1985 – K.G. Davey, The Female Reproductive Tract

1993 – V. Hartenstein, Atlas of Drosophila Development

2011 – R.I. Bailey, P. Innocenti, E.H. Morrow, U. Friberg, A. Qvanstrom. Female Drosophila melanogaster Gene Expression and Mate Choice: The X Chromosome Harbours Candidate Genes Underlying Sexual Isolation

Fig. 4 Wolfner et al. Figures

1997 – M.F. Wolfner, Drawing by S. Monsma, Tokens of Love: Functions and Regulation of Drosophila Male Accessory Gland Products (first depiction)

Version shown (2005 – M.F. Wolfner, S.W. Applebaum, Y. Heifetz, Gonadal Glands and their Gene Products)

1999 – D. M. Neubaum & M.F. Wolfner, Wise, Winsome, of Weird? Mechanisms of sperm storage in female animals.

2002 – O. Lung, U. Tram, C.M. Finnerty, M.A. Eipper-Mains, J.M. Kalb, M.F. Wolfner The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression

2007 – E.M. Adams, M.F. Wolfner, Drawings by A. Yori, Seminal Proteins but not Sperm Induce Morphological Changes in the Drosophila melanogaster Female Reproductive Tract During Sperm Storage

2009 – L.K. Sirot, B.A. LaFlamme, J.L. Sitnik, C.D. Rubinstein, F.W. Avila, C.Y. Chow, M.F. Wolfner, Drawing by J.L. Sitnik, Molecular Social Interactions: Drosophila melanogaster Seminal Fluid Proteins as a Case Study

2011 – M.F. Wolfner, Drawing by J.L. Sitnik, Precious Essences: Female Secretions Promote sperm Storage in Drosophila

2013 – M.F. Wolfner, C.D. Rubinstein, The Drosophila Seminal Protein Ovulin Mediates Ovulation Through Female Octopamine Neuronal Signaling

2015 – F.W. Avila, A. Wong, J.L. Sitnik, M.F. Wolfner, Don’t Pull the Plug! The Drosophila Mating Plug Perserves Fertility

Fig. 5 FRT Research Figures

2006 – P.D. Mack, A. Kapelnikov, Y. Heifetz, M. Bender, Mating-Responsive Genes in Reproductive Tissues of Female Drosophila melanogaster

2008 – A. Kapelnikov, P.K. Rivlin, R.R. Hoy, Y. Heifetz, Tissue Remodeling: A Mating-Induced Differentiation Program for the Drosophila Oviduct

Version shown (2016 – I. Carmel, U. Tram, Y. Heifetz, Mating Induces Developmental Changes in the Insect Female Reproductive Tract)

2012 – S.L. Schnakenberg, M.L. Siegal, M.C. Bloch Qazi, Oh, the Places They’ll Go: Female Sperm Storage and Sperm Precedence in Drosophila melanogaster

Fig. 6 Neurobiology Research Figures

1931 – H. Hertweck, Anatomie und Variabilitat des Nervensystems und der Sinnesorganne von Drosophila melanogaster (Meigen)

2006 – C.A. Middleton, U. Nongthomba, K. Parry, S.T. Sweeney, J.C. Sparrow, C.J.H. Elliott, Neuromuscular Organization and Aminergic Modulation of Contractions in the Drosophila Ovary

2009 – M. Hasemeyer, N. Yapici, U. Heberlein, B.J. Dickson, Sensory Neurons in the Drosophila Genital Tract Regulate Female Reproductive Behavior

2014 – K. Feng, M.T. Palfreyman, M. Hasemeyer, A. Talsma, B.J. Dickson, Ascending SAG Neurons Control Sexual Receptivity of Drosophila Females

Fig. 7 Developmental Research Figures

1978 – P.J. Bryant, Pattern Formation in Imaginal Discs

1983 – F. Epper, The Evagination of the Genital Imaginal Discs of Drosophila melanogaster

1997 – E.H. Chen and B.S. Baker, Compartmental Organization of the Drosophila Genital Imaginal Discs

2003 – B. Estrada, F. Casares, E. Sanchez-Herrero, Development of the genitalia in Drosophila melanogaster

Fig. 8 Microscopy

2009 – Y. Heifetz, P.K. Rivlin, Beyond the Mouse Model: Using Drosophila as a Model for Sperm Interaction with the Female Reproductive Tract

2012 – G. Newquist, 7th Prize Olympus BioScapes Digital Imaging Competition