Sperm morphology, adenosine triphosphate (ATP) concentration and swimming velocity: unexpected relationships in a passerine bird

Bennison, Clair; Hemmings, Nicola; Brookes, Lola; Slate, Jon; Birkhead, Tim R.

doi:10.1098/rspb.2016.1558

Cited by 40 publications

(52 citation statements)

References 36 publications

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“…For many different taxa, the effect of head length on sperm velocity is unclear. Our results are consistent with previous work that found no relationship between velocity and midpiece length but a positive association with head length in zebra finches (Bennison et al, ). However, an interspecific comparison across bird species found no effect of head:flagellum length on velocity but a significant effect of midpiece:flagellum length (Lüpold et al, ).…”

Section: Discussionsupporting

confidence: 94%

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Low‐mobility sperm phenotype in the domestic turkey: Impact on sperm morphometry and early embryonic death

Manier

Welch

Nispen

et al. 2019

Reprod Domestic Animals

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Contents The sperm mobility assay measures the ability of sperm to swim through a dense layer of Accudenz®, and the sperm mobility phenotype has been shown to predict fertility and other sperm performance traits in roosters and turkeys. In this study, we examined turkey sperm morphometry and rates of early embryonic death associated with high‐ and low‐mobility semen. We also assessed whether the hypo‐osmotic stress test, which evaluates the structural integrity of the sperm plasma membrane, may be used as a faster and simpler assay for sperm mobility and viability. We confirmed previous work that found that high‐mobility sperm are faster and swim more linearly than low‐mobility sperm, and that mobility traits were repeatable within males. In contrast to previous studies, we did not find higher rates of fertility, but low‐mobility sperm was associated with higher rates of early embryonic death, though this trend was not significant. High‐mobility sperm had longer sperm heads, explained by longer nuclei, despite shorter acrosomes. Although these sperm were faster, midpiece length and flagellum length did not differ between high‐ and low‐mobility sperm. Finally, mobility was not found to be associated with sperm performance in the hypo‐osmotic stress test.

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Section: Discussionsupporting

confidence: 94%

“…Moreover, zebra finches subject to oxidative challenge produce slower sperm with shorter midpieces (Tomáŝek, Albrechtová, Nĕmcová, Opatová, & Albrecht, ). At the same time, however, Bennison, Hemmings, Brookes, Slate, and Birkhead, () found that zebra finch sperm velocity was not correlated with midpiece length nor with ATP content.…”

Section: Discussionmentioning

confidence: 99%

Low‐mobility sperm phenotype in the domestic turkey: Impact on sperm morphometry and early embryonic death

Manier

Welch

Nispen

et al. 2019

Reprod Domestic Animals

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“…For instance, sperm may require more ATP to successfully collide with eggs at low viscosities, and their mitochondria produce ATP less efficiently at high temperatures (Blier et al, ). 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, ).…”

Section: Discussionmentioning

confidence: 99%

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

2019

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Global warming may threaten fertility, which is a key component of individual fitness and vital for population persistence. For males, fertility relies on the ability of sperm to collide and fuse with eggs; consequently, sperm morphology is predicted to be a prime target of selection owing to its effects on male function. In aquatic environments, warming will expose gametes of external fertilizers to the physiological effects of higher temperature and the physical effects of lower viscosity. However, the consequences of either effect for fertility, and for selection acting on sperm traits to maintain fertility, are poorly understood. Here, we test how independent changes in water temperature and viscosity alter male fertility and selection on sperm morphology in an externally fertilizing marine tubeworm. To create five fertilization environments, we manipulate temperature to reflect current‐day conditions (16.5°C), projected near‐term warming (21°C) and projected long‐term warming (25°C), then adjust two more environments at 21°C and 25°C to the viscosity of environments at 16.5°C and 21°C, respectively. We then use a split‐ejaculate design to measure the fertility of focal males, and selection on their sperm, in each environment. Projected changes in temperature and viscosity act independently to reduce male fertility, but act jointly to alter selection on sperm morphology. Specifically, environments resulting from projected warming alter selection on the sperm midpiece in ways that suggest shifts in the energetic challenges of functioning under stressful conditions. Selection also targets sperm head dimensions and tail length, irrespective of environment. We provide the first evidence that projected changes in ocean temperature and viscosity will not only impact the fertility of marine external fertilizers, but expose their gametes to novel selection pressures that may drive them to adapt in response if gamete phenotypes are sufficiently heritable. A free Plain Language Summary can be found within the Supporting Information of this article.

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“…The adaptive and functional significance of sperm size variation in birds has received considerable attention in recent years. More generally, sperm length is thought to be an important determinant of sperm swimming speed, an idea with some empirical support at both intra-and interspecific level in passerine birds (Lüpold et al 2009;Bennison et al 2016; but see Kleven et al 2009 andCramer et al 2015). More generally, sperm length is thought to be an important determinant of sperm swimming speed, an idea with some empirical support at both intra-and interspecific level in passerine birds (Lüpold et al 2009;Bennison et al 2016; but see Kleven et al 2009 andCramer et al 2015).…”

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confidence: 99%

Sperm head morphology is associated with sperm swimming speed: A comparative study of songbirds using electron microscopy

et al. 2018

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Sperm exhibit extraordinary levels of morphological diversification across the animal kingdom. In songbirds, sperm have a helically shaped head incorporating a distinct acrosomal membrane or "helical keel," the form and extent of which varies across species. The functional significance of this helical shape, however, remains unknown. Using scanning electron microscopy, we quantified inter- and intraspecific variation in sperm head morphology across 36 songbird species (Passeriformes: Passerida). Using phylogenetic comparative methods, we investigated the relationship between sperm head morphology and both sperm swimming speed and the frequency of extra-pair young (EPY). We found that species whose sperm had a relatively more pronounced helical form (i.e., long acrosome, short nucleus, wide helical membrane, and a more pronounced waveform along the sperm head "core") had faster-swimming sperm. We found no evidence of a relationship between interspecific variation in sperm head morphology and EPY, although we did find that among- and within-male variation in sperm head traits were negatively correlated with EPY. Applying principles of fluid mechanics, we discuss how the helical form of the sperm head may influence swimming speed, and suggest that further studies considering aspects of sperm morphology beyond sperm length are needed to improve our understanding of sperm structure-function relationships.

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Sperm morphology, adenosine triphosphate (ATP) concentration and swimming velocity: unexpected relationships in a passerine bird

Cited by 40 publications

References 36 publications

Low‐mobility sperm phenotype in the domestic turkey: Impact on sperm morphometry and early embryonic death

Low‐mobility sperm phenotype in the domestic turkey: Impact on sperm morphometry and early embryonic death

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

Sperm head morphology is associated with sperm swimming speed: A comparative study of songbirds using electron microscopy

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