A trade-off between thickness and length in the zebra finch sperm mid-piece

Abstract

The sperm mid-piece has traditionally been considered to be the engine that powers sperm. Larger mid-pieces have therefore been assumed to provide greater energetic capacity. However, in the zebra finch Taeniopygia guttata, a recent study showed a surprising negative relationship between mid-piece length and sperm energy content. Using a multi-dimensional approach to study mid-piece structure, we tested whether this unexpected relationship can be explained by a trade-off between mid-piece length and mid-piece thickness and/or cristae density inside the mitochondrial helix. We used selective plane illumination microscopy to study mid-piece structure from three-dimensional images of zebra finch sperm and used high-resolution transmission electron microscopy to quantify mitochondrial density. Contrary to the assumption that longer mid-pieces are larger and therefore produce or contain a greater amount of energy, our results indicate that the amount of mitochondrial material is consistent across mid-pieces of varying lengths, and longer mid-pieces are simply proportionately ‘thinner’.

Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology

“…Unfortunately, the exact energetic benefits of changes in midpiece morphology under warmer conditions are difficult to ascertain, since past studies have found it to have inconsistent relationships with sperm performance (Bennison, Hemmings, Brookes, Slate, & Birkhead, ) and have mostly focused on internal fertilizers with different reproductive biology to Galeolaria (but see Schlegel, Binet, Havenhand, Doyle, & Williamson, ). Nonetheless, shorter or wider midpieces could potentially reflect beneficial rearrangements in the internal organization of mitochondria (Mendonca et al, ). For instance, denser packing of mitochondrial membranes can allow ATP to be produced more efficiently (Demongeot, Glade, Hansen, & Moreira, ; Mannella, Lederer, & Jafri, ), and larger midpieces can store more energy to enhance sperm swimming performance (Firman & Simmons, ; Lüpold et al, , but see Bennison et al, ).…”

“…Nonetheless, shorter or wider midpieces could potentially reflect beneficial rearrangements in the internal organization of mitochondria (Mendonca et al, 2018). For instance, denser packing of mitochondrial membranes can allow ATP to be produced more efficiently (Demongeot, Glade, Hansen, & Moreira, 2007;Mannella, Lederer, & Jafri, 2013), and larger midpieces can store more energy to enhance sperm swimming performance (Firman & Simmons, 2010;Lüpold et al, 2009, but see Bennison et al, 2016).…”

“…For instance, sperm swimming speed is dictated by counteracting forces of thrust produced by the tail versus drag produced by the head and midpiece, which respectively house the nucleus and mitochondria (Humphries, Evans, & Simmons, 2008). Recent work also suggests that mitochondria produce energy (ATP) in proportion to midpiece size, allowing the midpiece to impact sperm swimming performance not only as a source of drag, but through its role in energy metabolism (Firman & Simmons, 2010;Fitzpatrick & Lüpold, 2014;Mendonca, Birkhead, Cadby, Forstmeier, & Hemmings, 2018). Evidence is therefore mounting that the reproductive physiology of natural populations may be susceptible to projected warming (Walsh et al, 2019) and that warming may generate novel opportunities for selection on reproductive traits.…”

Sperm gatekeeping: 3D imaging reveals a constricted entrance to zebra finch sperm storage tubules

“…However, even without contractility, the narrow SST orifice (mean diameter of about 315 3 µm), with the added obstruction of microvilli (1-2 µm in length, [52]) could restrict 316 the rate of sperm (mean diameter at mid-piece -~0.6 µm [59]) entering and exiting 317 the SST, thereby providing a mechanism by which sperm storage and release can be 318 regulated. This, combined with the fact that sperm do not appear to actively swim 319 inside or on immediate release from the tubules, supports the idea that avian SSTs 320 play an active and selective role in sperm storage, regulating sperm uptake and 321 release and suppressing motility [33][34][35][36][37][38].…”

The mesoSPIM initiative: open-source light-sheet microscopes for imaging cleared tissue

“…For example, the openSPIM project is highly successful as a tool to train microscopists on how to build and use a light-sheet microscope. However, only a small fraction [16][17][18][19][20][21][22] With the mesoSPIM initiative, we hope to provide a mesoscopic imaging instrument for cleared tissue en par or better than existing options. The setup is thus suitable for research groups or imaging facilities in search of alternatives to the existing palette of commercial instruments.…”