Disputing Lamarckian epigenetic inheritance in mammals

Lamarckian inheritance is the theory that an organism can pass on phenotypes that
it acquired during its lifetime to its offspring. This theory was first postulated
at the start of the 19th century, but by the end of that century the model of genetic
inheritance, from Darwin and Mendel, became preferred. Over the past decade, a handful
of studies carried out in mammals have provided support for the idea that exposure
to environmental events can drive phenotypic changes that are inherited for more than
one generation, and that this occurs through epigenetic mechanisms. One of the key
studies driving recent support for Lamarckian inheritance 2] reported that the exposure of pregnant female rats to the endocrine disruptor vincozolin
affected male fertility in subsequent generations and that these effects were associated
with epigenetic changes in the germ line.

A few independent studies of a range of environmental exposures, such as to bisphenol
A, also reported that the resulting phenotype was associated with epigenetic changes
in the next generation 3]. Evidence that such effects last for more than one generation has been inconclusive
(reviewed in 4]-6]). In some instances, effects have been reported following exposure of the male parent
to a ‘stress’ 7],8]. For example, offspring of male mice that had been fed a low-protein diet showed
changes in the expression of genes involved in cholesterol biosynthesis and changes
in DNA methylation 8]. In parallel studies of human populations, it has been suggested that abnormal phenotypes
caused by stressors, such as low nutrient intake, might be passed on for many generations
through epigenetic marks on the gametes of one parent 9]-11]. From these studies, the hypothesis has emerged that environmental ‘stress’ results
in epigenetic changes at some loci in the genome and that these can escape the epigenetic
reprogramming that normally occurs between generations, the end result being a Lamarckian
form of inheritance.

Although the topic is certainly controversial and stimulates robust discussions in
informal settings, studies that refute the idea are mainly absent from the literature.
It is very difficult to publish negative results, no matter how important those negative
results might be. The end result is that the published studies supporting Lamarckian
inheritance seem to be uncontested to those outside the field. As a result, many people
who are unfamiliar with the molecular sciences and who may be less able to critically
assess the evidence are getting an incomplete story.