Contributions to Zoology, 86 (4) – 2017Menno Schilthuizen; Rob Langelaan; Nicola Hemmings; Wesley van Oostenbrugge; Stefan Visser: An unexpected twist: Sperm cells coil to the right in land snails and to the left in song birds

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Discussion

Our results suggest that sperm cell chirality is fixed in two large clades of animals: exclusively dextral in Stylommatophora, and exclusively sinistral in Passeriformes. Although we see interspecific differences in the number of gyres, the height of the crest, and the extent to which the helical structure dominates along the length of the acrosome, nucleus, midpiece, and tail, we found no indication of any intra-individual, intraspecific or interspecific variability in the direction of coiling. For Stylommatophora, this finding is consistent with the dextral sperm cells previously reported in the land snails Amphidromus inversus Müller, 1774, Arion hortensis (Férussac, 1819), Deroceras reticulatum (Müller, 1774), Tandonia sowerbyi (Férussac, 1823), and Anguispira alternata (Say, 1816) (Schilthuizen and van Heuven, 2011, and references therein).

For the Passeriformes, sinistrality has previously also been reported in, for example, Hirundo rustica Linnaeus, 1758, Turdus merula Linnaeus, 1758, Fringilla coelebs Linnaeus 1758, Sturnus vulgaris Linnaeus, 1758, and Poephila acuticauda (Gould, 1839) (Retzius, 1909; Vernon and Woolley, 1999; Hermosell et al., 2013; Rowe et al., 2015).

In contrast, a small number of papers depict stylommatophoran spermatozoa as sinistral helices (e.g., Maxwell, 1975, for Cornu aspersum (Müller, 1774), Selmi et al., 1989, for Oxyloma elegans (Risso, 1826)). Similarly, Birkhead and Immler (2007) depict a Passer domesticus (Linnaeus, 1758) sperm cell as a dextral helix. Because none of these papers explicitly state the chirality of their subjects, these inconsistencies could, in fact, be the result of inadvertent mirror-imaging of the scanning-electron micrographs. A more reliable deviation from our observations is Hickman (1931: 265), who states that in the amber snail Novisuccinea ovalis (Say, 1817), ‘there is no uniformity of direction of the spirals. [...] Out of many specimens examined, I find that the spirals may go in either a left or a right direction from head to tail, and that one condition is about as common as the other’. If confirmed by additional observations, this would suggest fixed coiling direction may be lost in some stylommatophoran lineages.

Despite the aforementioned deviations, and pending further investigations to augment the number of species and individuals sampled, we tentatively stress the uniformity in coiling direction of sperm cells in Stylommatophora and Passeriformes. It is tempting to speculate that such cellular homochirality is due to the same chiral cytoskeletal elements, such as actin filaments, that set in motion whole-body homochirality in the zygote (Levin and Palmer, 2007). Although, during spermiogenesis, the sperm cell nucleus retains little more than a near-crystalline DNA-histone-protamine complex, the acrosome, which, especially in birds, forms a considerable portion of the spiral sperm head, is known to contain actin filaments (e.g., Breitbart et al., 2005).

Another potentially relevant observation is that the sinistral and dextral sperm cells in birds (deuterostomes) and snails (protostomes) parallels the inversion of the antero-posterior and dorso-ventral axes in deuterostomes. The result in whole-body chirality is that the right of protostomes becomes the left in deuterostomes.

However, we doubt that such a one-to-one relation exists between spermatozoon homochirality and organismal homochirality. Two previous studies, by Selman and Waddington (1953) and Schilthuizen and van Heuven (2011), showed that snail species that are dimorphic for whole-body coiling direction (Radix labiata (Rossmässler, 1835) and Amphidromus inversus, respectively, which display both left-handed and right-handed shells), nonetheless always show dextral sperm. Similar studies have not yet been carried out in birds, where mirror-image reversal of the viscera is exceedingly rare (Palmer, 2004).

In conclusion, we suggest that a wider study of chirality in helical sperm cells in these and other taxa may prove a useful source for understanding symmetry breaking in development. We also suggest that studies of sperm morphology always explicitly record and identify the chirality of spiral structures and confirm that imaging methods did not yield inverted images.