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

Angela J Crean,Russell Bonduriansky,Anna M Kopps,Dustin Marshall

doi:10.1111/ele.12373

Abstract

Newly discovered non-genetic mechanisms break the link between genes and inheritance, thereby also raising the possibility that previous mating partners could influence traits in offspring sired by subsequent males that mate with the same female (‘telegony’). In the fly Telostylinus angusticollis, males transmit their environmentally acquired condition via paternal effects on offspring body size. We manipulated male condition, and mated females to two males in high or low condition in a fully crossed design. Although the second male sired a large majority of offspring, offspring body size was influenced by the condition of the first male. This effect was not observed when females were exposed to the first male without mating, implicating semen-mediated effects rather than female differential allocation based on pre-mating assessment of male quality. Our results reveal a novel type of transgenerational effect with potential implications for the evolution of reproductive strategies.

Highlights

Recent advances in our understanding of inheritance have revealed that offspring-parent resemblance cannot be explained solely by the transmission of parental genes
We found that the adult body size of offspring was influenced positively by the condition of females’ initial mate (‘first male’): offspring were ~ 0.5 SD larger when the female was initially mated to a high-condition male than when the female was initially mated to a low-condition male (Fig 3a)
Our results show that it is possible for a male to transmit features of his phenotype via non-genetic semen-borne factors to his mate’s subsequent offspring sired by another male

Summary

Introduction

Recent advances in our understanding of inheritance have revealed that offspring-parent resemblance cannot be explained solely by the transmission of parental genes (see recent reviews: Danchin et al 2011; Bonduriansky 2012). Before the advent of modern genetics, many biologists believed that a male can leave a mark on his mate’s body, causing the female’s subsequent offspring to resemble their mother’s first mate, despite being sired by another male (Rabaud 1914; Ewart 1920). 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 1979). Classic discussions of telegony focused on effects carried over from one gestation to the similar mechanisms could enable males who do not sire any offspring to influence the development of future offspring sired by other males

Methods

Results

Conclusion