Abstract
The classical view of “pheromone”—an air-borne chemical signal—is challenged by the camelids in which ovulation is triggered by ß-nerve growth factor carried in seminal plasma, effectively extending the pheromone concept to a new medium. We propose further extension of “pheromone” to include a separate class of seminal fluid molecules that acts on the female reproductive tract to enhance the prospect of pregnancy. These molecules include transforming growth factor-ß, 19-OH prostaglandins, various ligands of Toll-like receptor-4 (TLR4), and cyclic ADP ribose hydrolase (CD38). They modulate the immune response to “foreign” male-derived histocompatibility antigens on both sperm and the conceptus, determine pre-implantation embryo development, and then promote implantation by increasing uterine receptivity to the embryo. The relative abundance of these immunological molecules in seminal plasma determines the strength and quality of the immune tolerance that is generated in the female. This phenomenon has profound implications in reproductive biology because it provides a pathway, independent of the fertilizing sperm, by which paternal factors can influence the likelihood of reproductive success, as well as the phenotype and health status of offspring. Moreover, the female actively participates in this exchange—information in seminal fluid is subject to “cryptic female choice,” a process by which females interrogate the reproductive fitness of prospective mates and invest reproductive resources accordingly. These processes participate in driving the evolution of male accessory glands, ensuring optimal female reproductive investment and maximal progeny fitness. An expanded pheromone concept will avoid a constraint in our understanding of mammalian reproductive biology.
Highlights
Fos expression studies have shown that, in the first 2 h of male exposure, cells are activated in the arcuate nucleus (ARC), the ventromedial nucleus of the hypothalamus (VMH) and the organum vasculosum of the lamina terminalis (OVLT); by 6 h after male exposure, cells in the preoptic area (POA) are activated [5]; 3
Seminal fluid carries molecular agents that act in the female reproductive tract to alter female physiology in a most fundamental way to promote reproductive success, and these effects go well beyond the induction of ovulation
We contend that the chemical components of seminal fluid meet the definition of “pheromone”— they act outside the body of the originating male to affect the HPG axis of the female but to change her immune system and enhance the prospect of a successful pregnancy
Summary
While the theme of this special issue of Frontiers in Veterinary Science is focused clearly on signals transferred from males to females in semen, we would like to add an extra dimension to the discussion—the concept of “pheromone.” The original approach to male-female chemical signaling emerged from the field of entomology, for which pheromones were defined by Karlson and Lüscher in 1959 [1]: “. . . substances which are secreted to the outside by an individual and received by. We will use the “ram effect” as a primary example of a pheromone that has profound effects on mammalian reproduction (review: 2). It involves an olfactory signal from novel rams that activates the hypothalamic-pituitarygonadal (HPG) axis of anovulatory ewes, leading to ovulation within a few days. Molecules that are evolved signals, in defined ratios in the case of multiple component pheromones, which are emitted by an individual and received by a second individual of the same species, in which they cause a specific reaction, for example, a stereotyped behavior or a developmental process.”. The question we pose here is: can we stretch the pheromone definition beyond olfactory signals to include semen, the complex biological and chemical mixture that is transmitted from males to females at mating?
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