What Is Lost in the Weismann Barrier?

Abstract

The Weismann barrier has long been regarded as a basic tenet of biology. However, upon close examination of its historical origins and August Weismann's own writings, questions arise as to whether such a status is warranted. As scientific research has advanced, the persistence of the concept of the barrier has left us with the same dichotomies Weismann contended with over 100 years ago: germ or soma, gene or environment, hard or soft inheritance. These dichotomies distract from the more important questions we need to address going forward. In this review, we will examine the theories that have shaped Weismann's thinking, how the concept of the Weismann barrier emerged, and the limitations that it carries. We will contrast the principles underlying the barrier with recent and less recent findings in developmental biology and transgenerational epigenetic inheritance that have profoundly eroded the oppositional view of germline vs. soma. Discarding the barrier allows us to examine the interactive processes and their response to environmental context that generate germ cells in the first place, determine the entirety of what is inherited through them, and set the trajectory for the health status of the progeny they bear.

Keywords: Weismann barrier; germ cells; germline; soma; transgenerational epigenetic inheritance.

Figure 1

Illustration of Weismann’s vital units. Each chromosome, or idant (A), is composed of several ids (dark blue) (B) that are inherited intact from the parental germ cells within the germ plasm. Each id is composed of determinants (C) that are arranged in a particular architecture. Each determinant corresponds to a specific cell type in an organism and contains a particular assemblage of biophors (D), a group of molecules that, when released from the nucleus and into the cytoplasm, provide the starting material from which cellular components develop.

Figure 2

According to Weismann, cells can undergo either ordinary (A) or embryogenic divisions (B). (A) Ordinary divisions produce daughter cells with chromosomes bearing vital unit composition identical to the parental cell and maintain the germ plasm intact from the zygote through mature germ cells. (B) Embryogenic divisions produce daughter cells with chromosomes that bear different determinants in their ids depending upon their destined cell lineage.

Figure 3

Model of germ cells in the absence of the Weismann barrier. Within the germ cell (purple), interactions between the nuclear and cytoplasmic components integrate signals from the surrounding somatic gonad cells, which themselves are responsive to signals from the germ cell. The germ cells and somatic gonad cells are situated within a larger somatic environment that is in turn influenced by the extraorganismal environment.