Sperm competition and sex allocation in mammalian males : integrating reproductive physiology and evolutionary ecology.

Sexual selection is a key driving force on male reproductive traits developed as adaptations to both pre-copulatory and post-copulatory competition. Sperm competition is the post-ejaculatory equivalent of pre-mating male-male competition. Relative testes mass is commonly used as a proxy of sperm competition, as larger testes which produce more spermatozoa should result in higher paternity success. However, the testis has functional roles beyond sperm production, and responds to various selection pressures other than sperm competition. Thus, in this thesis I explored how a father may invest in spermatozoa quantity and spermatozoa quality to construct a viable and competitive ejaculate, in both sperm competition and sex allocation. I firstly investigate whether diverse social mating systems and thus implied sperm competition intensity, predict testes mass (chapter 2). I show that relative testes mass varies between species of mole-rats with different sperm competition intensity in most, but not all cases which suggests relative testes mass does not always follow expected patterns. Based on the conclusions of chapter 2, I describe the multifaceted functions of testes that are not necessarily indicative of sperm competition, and review the assumptions underlying studies of sperm competition, including whether testes mass is a reliable measure of sperm competition intensity (chapter 3). I also present literature-based evidence that the epididymis may consist of mechanistic control of paternal sex allocation as mammalian spermatozoa are dimorphic cells and speculate that sperm sex may be a trait associated with sperm competition where a father may be more advantaged by producing offspring of one sex over the other. When constructing a viable ejaculate, spermatozoa production (quantity) via the testis, and spermatozoa maturation (quality) via the epididymis, are distinct processes. Collating recent advances from studies of mammalian male reproductive physiology, I propose extending measures of sperm competition beyond testes mass and sperm production alone. I introduce the epididymis as an overlooked contributor to sperm competition, to better reflect the different aspects of an individual male’s physiological capacity to compete for paternity (chapter 4). While differences between mole-rat species were non-significant, I suggest that males are likely capable of allocating resources within the reproductive tract to enhance sperm quality during maturation of spermatozoa during epididymal transit. How the epididymis responds to sperm competition has previously been unexplored and mechanistic understanding of how (and where) ejaculate X-Y ratios arise has been undetermined. Therefore, I investigate the potential for paternal control over offspring sex via biasing of the spermatozoa X-Y ratio (ratio of X-chromosome bearing spermatozoa to Y-chromosome bearing spermatozoa) within the epididymis of the mouse. I demonstrate the variable nature of spermatozoa within the male reproductive tract and show that sperm sex ratios are not fixed to the 50:50 meiotic ratio (chapter 5). I show that variable X-Y ratios occur earlier during epididymal transit than previously known and are not static throughout epididymal transit. I also show that reactive oxygen species (ROS) level varies between spermatozoon types and increases throughout epididymal maturation. I summarise my thesis in the general discussion to highlight how each chapter builds upon the previous chapter to shed light on the diverse functions of the mammalian male reproductive tract for producing an ejaculate. I conclude by suggesting future directions that may enable empirical tests of sperm competition in mammals to draw causative conclusions, by considering the entire process of constructing a viable ejaculate through a physiological frame of reference