Male gamete morphology in relation to swimming velocity and fertilisation microenvironment

Simpson, Julia Louise

Abstract

The heterogeneity of spermatozoa has been widely used to inform phylogenetic relationships among taxa, yet the reason such diversity has evolved, in relation to the sperms primary functional role in fertilisation and reproduction, is not well understood. Research into the evolutionary significance of sperm morphology is concomitant with the study of sexual selection and the evolution of the biological diversity of life. The formulation of sperm competition theory in the 1970s provided a new insight for the study of sexual selection and the development of the field of sperm biology. The idea that males not only competed for access to females but that, through direct competition, spermatozoa of individual males were also in competition to fertilise the maximum number of eggs was a revolutionary concept.

An integral part of many sperm competition models is the assumption that there is a relationship between sperm morphology and swimming velocity in terms of fertilisation success. In addition to this it is further assumed that longer sperm swim faster than shorter sperm. During competitive mating, when the ejaculate from two or more males compete to fertilise a given set of eggs, longer and therefore faster, sperm should have a fertilisation advantage as they can reach and fertilise eggs first. However identifying the traits that make individual sperm more or less capable of successfully fertilising an egg remain largely unknown for most species. There has so far been little empirical support for a link between sperm morphology and swimming speed and mixed results regarding the importance of swimming speed when it comes to increasing fertilisation success.

Here, three aspects of sperm biology were investigated in order to clarify functional links between sperm morphology and velocity. Firstly, the influence that female gametes have on the swimming behaviour of both fresh and cryopreserved bovine sperm was examined. Bovine samples were used because it is known that in the bovidae family, female gametes release chemoattractans which appear to play a role in sperm guidance towards the oocyte (egg). Additionally, a large literature base regarding damage caused by cryopreservation of bovine sperm exists. The second topic of research focuses on cichlid fish. Cichlids from Lake Malawi have been underrepresented in the published literature in sperm biology despite being extensively studied in relation to other aspects of their biology. A phylogenetically controlled study into links between sperm morphology and velocity across mouthbrooding cichlids from Lake Malawi was therefore undertaken. All endemic cichlids in Lake Malawi are maternal mouthbrooders in which the female broods both eggs and fry inside her buccal cavity (a cavity inside the mouth of the female between the jaw and cheek). The functional significance of the buccal cavity is also important as the point of fertilisation for some species. Variation in sperm length has been found in cichlid species in Lake Tanganyika where substrate fertilisers have significantly longer sperm than species fertilising inside the buccal cavity. However, links between morphology and velocity have found little support when using traditional methods that rely on the calculation of mean measurements of sperm morphology and velocity. Here an experimental approach focusing on measurements from individual sperm whilst accounting for within-male variation was employed to investigate the extent to which links between sperm morphology and velocity to be revealed across species. The third area expands on the idea that fertilisation point will have an influence on sperm form and function and compares sperm data from three internally and three externally fertilising species. Once again measurements from individual sperm were used and within-male variation was included in the analysis.

The influence of chemoattractants on sperm swimming speed and direction are frequently omitted in the sperm competition literature, as are comparisons of the effects of sperm preservation methods such as cryopreservation. Such considerations are, in a large part left to articles on animal breeding and artificial insemination. It is however, widely acknowledged that chemoattractans do influence sperm motility in a range of taxa and that cryopreservation damages sperm. Whilst chemotaxis in bovine sperm was not detected in this study, variation in swimming characteristics of bovine sperm related to the method of preservation was observed. As cryopreservation appears to alter sperm behaviour it seems unlikely that observations of swimming velocity of fresh and cryopreserved sperm can be compared when considering relationships between sperm length and velocity. Information from both fresh and cryopreserved sperm is useful when considering links between sperm traits and fertilisation success but need to be considered independently.

Using comparative methods to investigate sperm traits across closely related species of cichlid fish no phylogenetic correlation for sperm traits was found. Furthermore, sperm morphology did not show any correlation with velocity across species. However, when within-male variation was accounted for, a relationship between sperm morphology and velocity was revealed. Interestingly the relationship was frequently a negative one, a novel finding despite numerous studies into sperm morphology-speed relationships. When the results from data comparing internal and externally fertilising species was considered negative relationships tended to be more prevalent in internally fertilising species. If this is a general trend, that shorter sperm swim faster in internally fertilising species, we could extrapolate that the negative relationships between sperm length and velocity found in the cichlid data set exhibit sperm morphology adapted for internal fertilisation. A larger sample size would be required to conclusively support this suggestion that could confirm Lake Malawi cichlids share a common point of fertilisation, within the buccal cavity, despite high levels of diversity found in other aspects of the speciation of these cichlids.

The findings of the work presented here highlight the negative influence cryopreservation has on sperm motility and that measurements of individual spermatozoa are vital if links between morphology and velocity are to be detected. The importance of sperm preservation method on the swimming behaviour, and by association the ability of the individual sperm to successfully complete fertilisation, requires further investigation to link the morphology and velocity of individual sperm to the method of preservation. This link would provide valuable insight into the structure of sperm subpopulations which are the most resistant to cryopreservation and therefore of most value for techniques such as artificial insemination. Using a new method for measuring individual sperm morphology and velocity whilst accounting for intra-male variation significant links between sperm morphology and velocity in a number of vertebrates and invertebrates were revealed. The data gathered here suggests that such links could be widespread across more species than current empirical work indicates. Furthermore, the direction of relationships between morphology and velocity appear to be revealing disparity between internally and externally fertilising species.

Citation

Simpson, J. L. (2012). Male gamete morphology in relation to swimming velocity and fertilisation microenvironment. (Thesis). University of Hull. Retrieved from https://hull-repository.worktribe.com/output/4214148

• Thesis Type: Thesis
• Deposit Date: May 31, 2013
• Publicly Available Date: Feb 22, 2023
• Keywords: Biological sciences
• Public URL: https://hull-repository.worktribe.com/output/4214148
• Additional Information: Department of Biological Sciences, The University of Hull
• Award Date: Nov 1, 2012