Speciation by physiological selection of environmentally acquired traits

A chance mutation affecting a single or extremely few individuals in a continuous population will be quickly diluted through interbreeding. Charles Darwin fully appreciated this difficulty with relying on natural selection alone, and suggested an enabling role for geographical isolation in the origin of species. However, Darwin also believed in evolution by the inheritance of acquired traits and in populations of interbreeding animals, both of which would need a different isolating mechanism to overcome dilution and play a role in animal evolution. Historically disputed, the inheritance of acquired characters is now increasingly accepted as a phenomenon, and Charles Darwin himself is acknowledged as closely pre‐empting the type of physiology necessary to mediate it in his hypothesis of ‘pangenesis’. In this article, we question how the inheritance of acquired traits might overcome the problem of dilution by interbreeding and contribute to evolution. Specifically, we describe how Darwin's young protégé, George Romanes, developed ideas he discussed with Darwin and extended pangenesis to include a conceivable solution published after Darwin's death: physiological selection of fertility. In light of the ‘rediscovery’ of pangenesis, here we recount physiological selection as a testable hypothesis to explain how environmentally acquired characteristics could become coupled to the generation of species. figure legend Physiological selection is shown as a series of causes and effects. An environmental change causes epigenetic responses in a large fraction of the population. A given epigenetic effect may have the direct or indirect consequence of impacting reproduction or fertility, such as by changing mating behaviour or post‐zygotic compatibility. If this effect on reproduction is positively discriminate, meaning exhibits some reference of like‐with‐like, either by trait‐bearing organisms differentially reproducing with other trait‐bearing organisms, or less‐so with non‐trait‐bearing organisms, then the population will begin to diverge into sub‐species with different phenotypes.