Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct

Abstract

When spermatozoa from two or more boars are mixed and females inseminated, the resulting litters are often skewed in favour of one male but there is currently no satisfactory physiological explanation for this effect. However, to reach the oocytes, the spermatozoa must enter the oviduct where they are exposed to factors that modulate their activity. They either become sequestered within the oviductal sperm reservoir or bypass the reservoir and proceed towards the oocytes. The oviduct may therefore hold the key to mammalian sperm selection, thereby explaining why laboratory tests of sperm function, performed on whole ejaculates, are unable to account for the boar-specific skewing effects. We have previously shown that boar sperm motility is highly stimulated by bicarbonate, a naturally abundant component of oviductal fluid. Using motility-based sperm subpopulation analysis, we show here that the relative sizes of bicarbonate-responsive and unresponsive sperm subpopulations vary between individual boars. Proteins derived from oviduct epithelial plasma membranes suppress the activation response and modify sperm movement trajectories in a subpopulation-specific and dose-dependent manner. The suppression response varies between boars and some spermatozoa remain unsuppressed in the presence of oviductal proteins. When boars are ranked according to their susceptibility to bicarbonate-induced stimulation, rankings differ depending upon the presence or absence of oviductal proteins. The suppression response is not caused by inhibition of bicarbonate uptake; on the contrary this is enhanced by oviductal proteins. We suggest that the boar-specific and sperm subpopulation-specific interactions between sperm motility activation and suppression responses are likely to result in sperm selection before the spermatozoa meet the oocytes.