Inheritance of Acquired Traits in Insects and Other Animals and the Epigenetic Mechanisms that Break the Weismann Barrier

The credibility of the Weismann barrier has come into question. Several studies in various animal systems, from mice to worms, have shown that novel environmental stimuli can generate an altered developmental or behavioral trait that can be transmitted to offspring of the following generation. Recently, insects have become ideal models to study the inheritance of acquired traits. This is because insects can be reared in high numbers at low cost, they have short generation times and produce abundant offspring. Numerous studies have shown that an insect can modify its phenotype in response to a novel stimulus to aid its survival, and also that this modified phenotypic trait can be inherited by its offspring. Epigenetic mechanisms are likely at play but, most studies do not address the mechanisms that underlie the inheritance of acquired traits in insects. Here we first review general epigenetic mechanisms such as DNA methylation, histone acetylation and small noncoding RNAs that have been implicated in the transmission of acquired traits in animals, then we focus on the few insect studies in which these mechanisms have been investigated.

The Illusions of the Modern Synthesis

The Modern Synthesis has dominated biology for 80 years. It was formulated in 1942, a decade before the major achievements of molecular biology, including the Double Helix and the Central Dogma. When first formulated in the 1950s these discoveries and concepts seemed initially to completely justify the central genetic assumptions of the Modern Synthesis. The Double Helix provided the basis for highly accurate DNA replication, while the Central Dogma was viewed as supporting the Weismann Barrier, so excluding the inheritance of acquired characteristics. This article examines the language of the Modern Synthesis and reveals that it is based on four important misinterpretations of what molecular biology had shown, so forming the basis of the four Illusions: 1. Natural Selection; 2. The Weismann Barrier; 3. The Rejection of Darwin’s Gemmules; 4. The Central Dogma. A multi-level organisation view of biology avoids these illusions through the principle of biological relativity. Molecular biology does not therefore confirm the assumptions of the Modern Synthesis.

What Is Lost in the Weismann Barrier?

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.

Environmentally Induced Epigenetic Transgenerational Inheritance and the Weismann Barrier: The Dawn of Neo-Lamarckian Theory

For the past 120 years, the Weismann barrier and associated germ plasm theory of heredity have been a doctrine that has impacted evolutionary biology and our concepts of inheritance through the germline. Although August Weismann in his 1872 book was correct that the sperm and egg were the only cells to transmit molecular information to the subsequent generation, the concept that somatic cells do not impact the germline (i.e., the Weismann barrier) is incorrect. However, the doctrine or dogma of the Weismann barrier still influences many scientific fields and topics. The discovery of epigenetics, and more recently environmentally induced epigenetic transgenerational inheritance of phenotypic variation and pathology, have had significant impacts on evolution theory and medicine today. Environmental epigenetics and the concept of epigenetic transgenerational inheritance refute aspects of the Weismann barrier and require a re-evaluation of both inheritance theory and evolution theory.

Neuronal perception of the social environment intergenerationally controls germline development and generation time in C. elegans

ABSTRACTAn old and controversial question in biology is whether information perceived by the nervous system of an animal can ‘cross the Weismann barrier’ to alter the phenotypes and fitness of their progeny. Here we show that such intergenerational transmission of sensory information occurs in the model organism, C. elegans, with a major effect on fitness. Specifically, that perception of social pheromones by chemosensory neurons controls the post-embryonic timing of development of one tissue – the germline – relative to others in an animal’s progeny. Neuronal perception of the social environment thus intergenerationally controls the generation time of this animal.

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

The idea that there is an impenetrable barrier that separates the germline and soma has shaped much thinking in evolutionary biology and in many other disciplines. However, recent research has revealed that the so-called ‘Weismann Barrier’ is leaky, and that information is transferred from soma to germline. Moreover, the germline itself is now known to age, and to be influenced by an age-related deterioration of the soma that houses and protects it. This could reduce the likelihood of successful reproduction by old individuals, but also lead to long-term deleterious consequences for any offspring that they do produce (including a shortened lifespan). Here, we review the evidence from a diverse and multidisciplinary literature for senescence in the germline and its consequences; we also examine the underlying mechanisms responsible, emphasizing changes in mutation rate, telomere loss, and impaired mitochondrial function in gametes. We consider the effect on life-history evolution, particularly reproductive scheduling and mate choice. Throughout, we draw attention to unresolved issues, new questions to consider, and areas where more research is needed. We also highlight the need for a more comparative approach that would reveal the diversity of processes that organisms have evolved to slow or halt age-related germline deterioration.

The active role of spermatozoa in transgenerational inheritance

The active uptake of exogenous nucleic acids by spermatozoa of virtually all animal species is a well-established phenomenon whose significance has long been underappreciated. A growing body of published data demonstrates that extracellular vesicles released from mammalian somatic tissues pass an RNA-based flow of information to epididymal spermatozoa, thereby crossing the Weismann barrier. That information is delivered to oocytes at fertilization and affects the fate of the developing progeny. We propose that this essential process of epigenetic transmission depends upon the documented ability of epididymal spermatozoa to bind and internalize foreign nucleic acids in their nuclei. In other words, spermatozoa are not passive vectors of exogenous molecules but rather active participants in essential somatic communication across generations.