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How Environmental Contamination Has Changed the Course of Evolution

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Since the beginning of the chemical revolution 70 years ago, over 80,000 man-made chemicals have been created, some making their way into the environment and posing a serious risk to both human health and wildlife. These chemicals have been classified by the Endocrine Society as endocrine-disrupting chemicals (EDCs), and defined as "any exogenous chemical, or mixture of chemicals, that interferes with any aspect of hormone action." Today every body (human and animal) contains cocktails of these chemicals. This alarming fact is magnified by research demonstrating that exceptionally low levels of EDCs can be biologically relevant, especially if exposure occurs during critical life stages such as fetal development. The consequence is not toxicity and death but morbidity and compromised quality of life, including sterility. EDC exposure does not change the DNA itself but how DNA is regulated (a process called epigenetics), having an everlasting effect that potentially can affect all descendants.

What we want to discuss here is the effect of EDCs on evolution and show how present evolutionary theory, developed and codified prior to the chemical revolution, does not account for life in our contaminated world.

Evolutionary theory accounts for the process of change in life forms. It has had two epochs, with a third emerging. The first, known as Darwinian evolution (1800s), established the principle of change through natural selection. The second, called the modern synthesis (1900s), provided the units of heredity and their control, particularly change in DNA by recombination and mutation. The Mendelian geneticists effectively overthrew the Darwinian naturalists who emphasized the importance of the environment in shaping the phenotype. With the focus on genetics came the belief that evolution required fundamental changes to the unit(s) of heredity. The discovery of the structure of DNA gave credence to the idea that the genes themselves were the bricks from which the phenotype was built. This became the bulwark of the life sciences for the 20th century, with molecular biology and genetics the dominant disciplines in biology, a fact that continues today. Arguably the greatest discovery of the modern synthesis has been the remarkable conservation in the genetic code that links all animals.

We are entering the third epoch, what might be called the epigenetic synthesis, which combines elements of the previous iterations and incorporates environmental modulation of temporal and spatial control of gene expression without altering the underlying DNA sequence. This sea change is a consequence of the rediscovery of the importance of the environment, and how molecular epigenetics is the interface between the environment and gene regulation.

Prior studies paid at best lip service to the role of the environment, a perspective reified in the paradigm of gene-by-environment (G x E) interactions and its modern variants, such as genome-wide association studies, quantitative trait nucleotides, and whole-genome sequencing. This dogma holds that phenotypes, including disease, must have a genetic basis. However, with very rare exceptions, called monogenic diseases, which affect relatively few individuals, the genetic contribution to most diseases or traits is only about 2 to 5 percent, and multiple genes are involved in virtually every trait/disease. Even in monozygotic twins, a benchmark for assessing genetic risk complex in non-Mendelian disease, scientists have found only about 15 percent of breast cancers can be attributed to genetics, 25 to 45 percent for diabetes, 50 percent for schizophrenia, and 30 percent for bipolar disorder. As Bert Vogelstein and Nicholas Roberts have persuasively argued, genetic testing is not a panacea and relatively uninformative for most diseases. In fact, we now know that genetics is a subordinate player in virtually everything except for pathological conditions such as cancers. The conclusion we must face is that in most situations it is how the genome is regulated, not the nucleotide sequence itself, that is important.

It is time to think outside the box and develop de novo evolutionary principles and practices to better predict what the future holds. This new revolution should be firmly rooted in epigenetics. When defined broadly, epigenetics provides a very different perspective. It emphasizes how environmental experiences (whether internal and external, biotic and abiotic) modify the molecular factors and processes around DNA to regulate genome activity independent of the DNA sequence, essentially establishing an "imprint" that provides temporal and spatial control of genomic activity. The functional consequence of molecular epigenetic changes is that the "changed" organism responds differently to its environment.

It is important to distinguish the mechanisms underlying the epigenetic process and to go beyond the current emphasis on molecular processes (e.g., DNA methylation, histone modifications, long-noncoding RNAs, etc.). For the purpose of this essay, we can think of two major categories of change:

  1. Context- (or contact-) dependent epigenetic modifications (Ec) are caused by exposure to an environmental factor (including EDCs), social/behavioral factor, or other condition. So long as the causal agent bringing about the epigenetic modification persists, the epigenetic modification will manifest in each generation. Removal of the causative agent or addition of a different environmental factor (e.g., diet supplementation) can remediate the modification.
  2. Germline-dependent epigenetic modifications (Eg) are fundamentally different. Such modifications are mediated through the germline and hence will manifest in each generation in the absence of the causative factor. Both context- and germline-dependent epigenetic modifications have generational properties -- for example, passing from parent (father or mother) to the young -- but only Eg modification is truly transgenerational inheritance, because it is in the germline and does not require further exposure to be manifested.

Thus, epigenetic synthesis focuses on the interaction between germline-dependent (Eg) and context-dependent (Ec) modifications. That is, rather than G x E, etc., it is Eg x Ec that is likely to explain most of the variance observed between individuals and their fates. Beyond additivity or synergism, of greatest importance is the emergent property of the interaction -- that is, how transgenerational Eg modifications alter the organism such that it responds to proximate stimuli such as environmental stressors (Ec) in a different manner. In other words, in this new paradigm, the position of traditional genetics (the "G" of G x E) is not a factor; rather, it is how the genome is regulated that is the nexus. This is particularly true for humans, who are relatively recently evolved beings. Here it is their "shallow" (generations, or heritage) rather than their "deep" (millions of years, or phylogeny) ancestry that is important in the genetic sense.

Why is it necessary to develop a new paradigm? Evolution is the fabric of time, with reproductive success its warp and individual differences its weave. Change is marked by the advent, maintenance, and eventually the extinction of species. A case in point is the fossil record, a mosaic (fractured picture) of time past. Darwinian evolutionary theory predicted uniform but incremental (slow) change mediated by selection. However, the lack of such evidence of graded intermediate steps and, instead, the abrupt transition of forms in the fossil record, led to the theory of punctuated equilibria put forth by Niles Eldredge and Stephen Jay Gould, anticipated decades earlier by Rueben Ablowitz. They noted that transformative periods might mark periods of explosive change at both the species level as well as at the level of larger groups or clades, interspersed by prolonged periods of stasis with little or no change. Instrumental to the punctuated equilibrium theory was Richard Goldschmidt's macromutations or "hopeful monster" hypothesis in the mid-'60s, in which the rare phenotype so unlike any other extant at the time succeeds and paves the way for such transformative events.

We contend that environmental contamination by EDCs has created the conditions of incipient speciation. The world has been fundamentally transformed in the past seven decades -- a paleontological blink of an eye -- consistent with the upward trajectory of punctuated equilibrium. An epigenetic basis for this rapid transformation of form involving the silencing of transposable elements by environmental stressors has been proposed. Thus, we suggest that EDCs are a major category of environmental stressors that have created monsters "hopeful" to find mates.

In the modern synthesis, species formation was believed to result only after geographic separation and isolation of parts of the population, but it is now recognized that new species can arise in situ (i.e., sympatric speciation; e.g., changes in host-plant selection in apple maggots, and "resident" and transient forms of killer whales in the northeast Pacific). The controversy regarding these modes of speciation continues, but there has been a shift in evolutionary biology away from the isolationist perspective toward understanding the mechanisms that enable divergence of species in areas of sympatry. This has led to a reconsideration of the importance of interbreeding as an essential component of the "biological species concept," as many species can be made to interbreed under forced or artificial conditions when they would otherwise, given free choice, avoid such action.

While it is in an individual's best interest to avoid mating with a divergent species (resulting in no offspring or infertile offspring), Hugh Paterson has proposed that it is more important to select (through mutual agreement) the best mate within its own species, as happens in nature, thereby optimizing reproductive success. Further, the behavioral components of mating themselves are part of the complex process leading to successful reproduction. In vertebrates, the male's intromission and insemination induce behavioral and physiological responses in the female that may increase her receptivity, change her hormones, affect the probability of ovulation, and ultimately enhance the likelihood that his sperm will fertilize her eggs. Thus, both the physiological and behavioral components of mating are vulnerable to environmental EDCs. There is abundant evidence for perturbation of reproduction by EDCs, beginning with Rachel Carson's Silent Spring, which discusses the consequences of pesticides (such as DDT) in wildlife. What is not as commonly appreciated is the effects of EDCs on the behavioral aspects of reproduction, as well as other non-reproductive behaviors, in shaping evolutionary change.

Behavior is the leading edge of evolutionary change. That is, it is how the organism responds to its environment, including other individuals, that is the functional unit of selection. The brain, the organ of behavior, is one of the most important targets of EDCs, and we must consider their consequences on the intersection of brain, behavior, and the evolutionary process. There is clear evidence that in some instances, contamination compromises the reproductive capacity of individuals, and they cannot breed. There are many examples of such monsters in both wildlife and humans: feminized fish, multilimbed frogs, infants undergoing puberty. But it is also evident that reproduction continues in contaminated areas. Even if both sexes are compromised, they may encounter unaffected as well as affected individuals during the breeding season. Should affected individuals choose to mate with affected conspecifics, there may be no evolutionary impact if they are subfertile or infertile. However, if there were an asymmetry in mate preference (e.g., affected males mating with unaffected females, or vice versa), then the impact on the population would be significant, particularly if germline modifications (Eg) caused by EDCs are propagated. Until recently there have been few studies evaluating whether an individual's stimulus qualities and/or perception of suitable mates are modified by their progenitors' exposure to environmental contaminants. For example, starlings foraging in the winter on worms in sewage effluent filter beds receive significantly higher amounts of synthetic and natural estrogens and other EDCs than starlings foraging on worms found in garden soil. During the winter, captive male starlings were fed mealworms containing ecologically relevant levels of a mixture of EDCs found in worms in contaminated sites. The amount and complexity of song and the size of song nuclei (HVC) in the brain was assessed the following spring. Male song and HVC volume were increased in individuals receiving the mixture; these males also showed significantly lower immune function. Females preferred the more complex song of males that had received the EDC mixture. Thus, by selecting males with more complex song, the females were also selecting males who were immunocompromised.

A second example is that of exposure to the fungicide vinclozolin during the period of embryonic sex determination and gonadal differentiation in rats. This results in an acceleration of late-onset adult diseases, the phenotype of which is expressed by subsequent unexposed male progeny for three generations. Importantly, this phenotype is associated with DNA methylation changes in the sperm, a clear example of Eg. With Michael Skinner we recently demonstrated (and discussed in our previous blog in this series) how such Eg modifications change the behavior and brain transcriptome and mate preference behavior.

Real life, then, is a combination of Eg x Ec modifications. To our knowledge, this has been experimentally confirmed in animals for the first time in a model of transgenerational epigenetic modifications caused by ancestral vinclozolin exposure, with the unexposed descendants (F3 generation) subjected to a stressful environment in adolescence. We have demonstrated that in this context, Eg alters the brain, transcriptome, physiology, behavior, and metabolic activity in discrete brain nuclei in these descendants, and, importantly, the individuals respond very differently to their immediate environment (Ec). Thus, Eg x Ec can transform the essential elements of the phenotype. When applied to the real-life examples of contamination, such animals should be considered, until proven otherwise, as potential founder populations of new species.

Why is this important? The stress of contamination creates a bottleneck that only organisms that can adapt pass through. What is not appreciated is that such adapted species undergo a second bottleneck when the contamination is mitigated. Thus, "cleaning up" the environment represents further environmental stress, forcing further changes in species evolution. In other words, what develops is not the same organism as existed previously.

This means that your favorite species is not the same as it was 70 years ago. In the traditional evolutionary sense this is trivial, but in the real world, when contamination reigns, it is of fundamental importance.

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