Elsevier

Theriogenology

Volume 85, Issue 1, 1 January 2016, Pages 105-112
Theriogenology

Article
Sperm selection in the female mammalian reproductive tract. Focus on the oviduct: Hypotheses, mechanisms, and new opportunities

https://doi.org/10.1016/j.theriogenology.2015.07.019Get rights and content

Abstract

Research over the past 3 decades has caused a major shift in the way that the oviduct, or fallopian tube, is perceived. Previously, it was regarded as little more than the anatomic site for fertilization, where spermatozoa and oocytes meet as they travel in opposite directions. However, this view has been radically altered by the realization that both spermatozoa and oocytes elicit changes in the biochemical composition of oviductal fluid through the induction of novel gene expression. Moreover, it has also been shown that only a privileged sperm population, selected on the basis of multiple criteria, is permitted to enter the oviduct, where they are subjected to even more selection processes that control their motility and capacitation status, thus either inhibiting or facilitating their progress toward the oocyte. Even more recently, it has become apparent that the oviduct has some ability to differentiate the genetic signatures of X- and Y-bearing spermatozoa. Although how exactly this is achieved is unknown, it prompts us to speculate that the oviduct may also be capable of distinguishing other genetically encoded properties of individual spermatozoa and that there must ultimately be a huge payoff in terms of selective animal breeding.

Introduction

Sperm transport in the mammalian female reproductive tract has long been regarded as a race toward the oocyte(s), so that fertilization rate is biased in favor of the fastest swimmers. However, over the past 10 to 20 years, there has been a growing realization that the process of sperm transport is mediated by a far more complex series of interactions between the spermatozoa and the female reproductive tract and that the “sperm race” is no longer a tenable hypothesis. In vitro and in vivo studies have revealed that sperm behavior is modulated by physical and biochemical interactions with the cells lining the female reproductive tract and the mucous fluids that constitute the environment. The high viscosity of these fluids is of special significance because they can either inhibit or permit the passage of spermatozoa by altering the characteristics of their flagellar movement [1] and their beat frequency. The high viscosity also tends to make the spermatozoa swim near to available surfaces, and the female tract architecture has evolved multiple folds and grooves through which the spermatozoa can swim. In fact, recent evidence has demonstrated that the combined effects of viscous fluids and microgrooves in parts of the female reproductive tract provide significant degrees of selectivity, allowing the passage of spermatozoa but preventing infectious microorganisms from reaching the oviduct [2], [3]. Shortly after insemination, the female reproductive tract responds to spermatozoa by altering the suite of proteins it produces, thus also changing the physiological and biochemical environment. In fact, when spermatozoa enter the female reproductive tract, they elicit feedback responses from the adjacent epithelial cells, which in turn affect sperm storage, motility, survival, and capacitation.

The female reproductive tract is highly differentiated into distinct anatomic regions, and it is therefore clear that individual spermatozoa must experience interactions with different environments as they make their way toward the oocyte. Sperm deposition in pigs occurs directly into the uterus and involves the ejaculation of a large fluid volume (approximately 2–300 mL) over a period of 5 to 10 minutes. After ejaculation, the vaginal region of the cervix is believed to act as a filter-barrier against the external environment [4], and peristaltic uterine contractions push the spermatozoa toward the uterotubal junction (UTJ). At this stage, some components in seminal plasma exert direct effects on the ovaries, advancing the onset of ovulation by several hours [5]. Even before they reach the UTJ, the spermatozoa are eliciting local immunologic responses and some degree of sperm selection takes place, mediated, among other factors, via polymorphonuclear leukocytes (PMN) [6].

Section snippets

Sperm selection at the uterotubal junction and oviductal isthmus

Once the spermatozoa reach the UTJ, which represents a physical barrier, the next stage of their journey toward the oocyte(s) involves entering the oviduct and experiencing up to 40 hours of storage in contact with epithelial cells of the oviductal isthmus. In fact, the UTJ itself represents a significant sperm storage region in pigs, and it is likely that a further degree of sperm selection also takes place here. As pointed out by Hunter [7], viscous glycoproteins accumulate in the porcine

Sperm DNA and oviductal interactions

If this interpretation is correct, both the vanguard and oviductal spermatozoa should exhibit characteristics that mark them out as being “superior” to the unselected bulk populations. Ultrastructural studies of the pig oviduct in vivo support the view that the selected and membrane-bound spermatozoa possess intact plasma membranes [37], [38], but it is difficult to validate this view directly from these in vivo observations. Nevertheless, a significant study by Ardón et al. [39] has shown that

Oviductal responses to sperm entry

Once the spermatozoa reach the oviduct, they stimulate de novo gene transcription and protein synthesis. This was first noticed in studies of sperm interactions with in vitro–cultured bovine oviductal cells [60], at a time before the advent of proteomic technologies when it was not possible to identify the novel proteins. A later study in mice found that insemination induced de novo gene transcription in the female reproductive tract, stimulated specifically by spermatozoa and not by seminal

Can the oviduct distinguish the genetic properties of spermatozoa?

An important body of literature supports the hypothesis that females exert postcopulatory control over the quality of the fertilizing spermatozoon, via a mechanism known as “cryptic female choice” [76], [77]. The meaning of “quality” in this context is believed to encompass more than basic aspects of sperm function and invokes selective processes on the basis of the genetic attributes of the individual males [78], [79]. Observations that sperm proteins evolve more rapidly than somatic cell

Sex-specific sperm selection in vivo—is it possible?

The evidence cited previously shows that there are numerous potential mechanisms for controlling sperm progression through the female reproductive tract. Immediate and dramatic control of sperm physiology within the oviduct can be exerted by local concentrations of small molecules such as bicarbonate [103], calcium, [104], [105] and nitric oxide [106] as well as by secreted proteins [107]. However, there is little to suggest at present that these effects are preferentially exerted on sperm

Conclusions

In this article, we have aimed to show that sperm selection within the female reproductive is mediated by multiple factors, including the physical characteristics of the variably viscous fluid milieu in which the spermatozoa are bathed and the biochemical components that it contains. Moreover, binding interactions between spermatozoa and adjacent epithelial cells stimulate novel gene expression and therefore elicit changes to the biochemical environment itself. This may result in differential

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