Telegony, the Sire Effect and non‐Mendelian Inheritance Mediated by Spermatozoa: A Historical Overview and Modern Mechanistic Speculations

Abstract

Telegony is the belief that the sire first mated to a female will have an influence upon some of that female's later offspring by another male. Although the reality of telegony was acknowledged by such authorities as Darwin, Spencer, Romanes and many experienced breeders, it has been met with scepticism because of Weismann's unfavourable comments and negative results obtained in several test experiments. In this article, alleged cases of telegony are provided. A search of the literature of cell biology and biochemistry reveals several plausible mechanisms that may form the basis for telegony. These involve the penetration of spermatozoa into the somatic tissues of the female genital tract, the incorporation of the DNA released by spermatozoa into maternal somatic cells, the presence of foetal DNA in maternal blood, as well as sperm RNA-mediated non-Mendelian inheritance of epigenetic changes.

Revisiting telegony: offspring inherit an acquired characteristic of their mother's previous mate

“…Potential mechanisms of telegony include penetration of maternal somatic cells by sperm, foetal genes in mother's blood, and the ability of RNA to program genome rearrangement (Liu , ). In addition, males provide the female with a suite of proteins and other molecules in the seminal fluid (Avila et al .…”

“…Potential mechanisms of telegony include penetration of maternal somatic cells by sperm, foetal genes in mother's blood, and the ability of RNA to program genome rearrangement (Liu 2011(Liu , 2013. In addition, males provide the female with a suite of proteins and other molecules in the seminal fluid (Avila et al 2011), the concentration and composition of which can be altered by the male's environment (Wigby et al 2009;Perry & Rowe 2010;Sirot et al 2011).…”

“…This hypothesised phenomenon, dubbed ‘telegony’ by August Weismann, was rejected in the early 20th century because it lacked unequivocal empirical support and was deemed incompatible with Mendelian genetics (Burkhardt ). However, recent discoveries have revealed the existence of molecular and physiological mechanisms that have the potential to mediate telegony (Liu , ). Although classic discussions of telegony focused on effects carried over from one gestation to the next, similar mechanisms could enable males who do not sire any offspring to influence the development of future offspring sired by other males.…”

Darwin and Mendel today: a comment on “Limits of imagination: the 150th Anniversary of Mendel’s Laws, and why Mendel failed to see the importance of his discovery for Darwin’s theory of evolution”

“…Today, it is widely recognized that cells can actively release into the extracellular environment diverse types of molecules, such as circulating DNA, mobile RNAs, and prions, which agree beautifully with Darwin's imagined gemmules (Liu 2008). There is also striking evidence for telegony (Liu 2011;Crean et al 2014), graft hybridization (Liu 2006;Fuentes et al 2014), and the inheritance of acquired characters (Liu 2007;Rechavi et al 2014), which Darwin's Pangenesis supposedly explains. We believe that Darwin's Pangenesis, if and when sustained or rediscovered, would have a tremendous impact on the development of genetics and evolution (Liu and Li 2014).…”

Inheritance of acquired characters in animals: A historical overview, further evidence and mechanistic explanations

“…-S. Liu mother. It has been supposed that the circulating DNA released by the hybrid embryo is transferred into the mother's body by circulation, and later is incorporated into the mother's subsequent hybrid embryo by another male, thus being able to influence the characteristics of the subsequent offspring (Liu 2011).…”