Gamete compatibility genes in mammals: candidates, applications and a potential path forward

Abstract

Fertilization represents a critical stage in biology, where successful alleles of a previous generation are shuffled into new arrangements and subjected to the forces of selection in the next generation. Although much research has been conducted on how variation in morphological and behavioural traits lead to variation in fertilization patterns, surprisingly little is known about fertilization at a molecular level, and specifically about how genes expressed on the sperm and egg themselves influence fertilization patterns. In mammals, several genes have been identified whose products are expressed on either the sperm or the egg, and which influence the fertilization process, but the specific mechanisms are not yet known. Additionally, in 2014 an interacting pair of proteins was identified: 'Izumo' on the sperm, and 'Juno' on the egg. With the identification of these genes comes the first opportunity to understand the molecular aspects of fertilization in mammals, and to identify how the genetic characteristics of these genes influence fertilization patterns. Here, we review recent progress in our understanding of fertilization and gamete compatibility in mammals, which should provide a helpful guide to researchers interested in untangling the molecular mechanisms of fertilization and the resulting impacts on population biology and evolutionary processes.

Keywords: cryptic female choice; gamete compatibility; mate compatibility; post-copulatory sexual selection.

Figure 1.

Overview of egg structure. The ovulated egg is surrounded by a hyaluronic acid matrix, which contains cumulus cells. The zona pellucida (ZP) separates the cumulus cells from the egg. The perivitelline space is the space between the ZP and the membrane of the egg. Figure drawn from [8,31].

Figure 2.

Overview of major structures, sites and transport/guiding processes involved in fertilization. Although there is variation across mammals, this is meant to represent generic features of mammalian reproduction. Figure drawn from [49,51].

Figure 3.

Sperm structure and capacitation. Diagram of the sperm head containing the nucleus with the haploid genome, and the acrosome, which is a secretory organelle. The acrosome has two membranes, an inner and outer. Capacitation causes multiple physiological changes in the head, acrosome and tail of the sperm, which is necessary for fertilization. Figure drawn from reference [8].

Figure 4.

Changes to spermatozoa during the acrosome reaction. The inner acrosomal membrane is exposed allowing the spermatozoa to bind to and penetrate the zona pellucida, and to bind to the egg plasma membrane. Figure drawn from [8,37].

Figure 5.

Major steps in fertilization. (1) Spermatozoa undergo the acrosome reaction probably prior to reaching the cumulus mass [71,72]; (2) spermatozoa penetrate the cumulus cells; (3) spermatozoa binds to the zona pellucida; (4) sperm moves through the zona pellucida into the perivitelline space; (5) sperm binds to the egg plasma membrane; (6) sperm fuses with the egg plasma membrane. Note that binding (step 5) and fusion (step 6) are distinct processes, and studies have shown that sperm can bind to the plasma membrane without fusing with it. Figure drawn from [7].