Over the last 100 years, species extinction has largely been a result of man-induced habitat destruction and over-exploitation. Recently, habitat destruction has taken on a whole new meaning by the addition of man-made chemicals in concentrations that range upwards from barely detectable. The habitat may still, on the surface, look untouched, but the new chemicals in these formerly pristine systems, have the capacity to change the evolutionary fate of many of the earth's species. These man-made chemicals found in the food, air and water utilized by many animal species (including our own) can accumulate in the fatty tissues and work their way up the food chain to become concentrated more than a millionfold above background levels in the top predators such as humans, polar bears, stellars sea lions, eagles, giant tuna and many others. In mammals, these contaminants can then be passed on to the next generation via the mother by the conversion of the chemical-laiden fat to milk. In fish, birds and amphibians, the egg yolk can transmit the chemicals from the mother to her offspring. The offspring not only receives nourishment, but also a chemical dose many times greater than normal. Thus the infant starts life with an unusually high background level of contamination that will only increase during its lifetime. Thus the chemical dose received in infancy will increase with each succeeding generation. Recent research published by Monteiro and Furness demonstrated by feather analysis of samples collected from 1886 to 1994 that mutagen methyl mercury has been increasing in oceanic seabirds living in the pristine Azores, Madeira and Salvages islands at about 5% per year in the petrels and 2% per year in the shearwaters. The different rates reflect alternate dietary preferences for fish species belonging to food chains with different contamination levels. At what level of contamination does the amount genetic damage increase in these isolated populations as a consequence of the build up of bioaccumulated mutagens? Once such a critical stage is reached and genetic damage increases, the genetic structure of these bird populations may become so affected that general reproductive failure results.
What about human and other animal populations that are more directly exposed to these environmental mutagens, such as urban city dwellers, smokers and fish living in effluent influenced water? The genetic effects of these chemicals in isolation or in mixtures is only just now beginning to be understood through the utilization of new methodologies recently developed in medical science and molecular genetics. The endocrine disrupters, endocrine mimics, genetic diseases such as cancer and other factors all can have an impact on the fitness of a population and ultimately its genetic structure. Those individuals with the greatest fitness in the chemical laden habitats will leave the most offspring and the genes which enable their success will increase in frequency. Theodorakis and Shugart of the Oak Ridge National Laboratory in Tennessee looked at mosquitofish in ponds with and without radioactive contamination. Fish from the contaminated ponds were much more genetically similar than those from uncontaminated ponds, even though one of the contaminated populations had originated from fish in one of the uncontaminated ponds. They then transferred 25 fish from the uncontaminated pond to the contaminated pond. The seven survivors had genetic constitutions similar to the resistant resident population.
This process of selection is not without a cost to the population. Unger and Vogelbein and their colleagues at the Virginia Institute of Marine Science showed that the mummichog, a small fish inhabiting Chesapeake Bay, can evolve resistance to carcinogenic polycyclic aromatic hydrocarbons (PAH) found in the sediment. Non-resistant mummichog embryos and adults suffer 100% mortality when exposed to the contaminated sediments. The PAH resistant fish, when exposed to a noncontaminated environment were much more susceptible to disease than when reared under the contaminated conditions. Many rare, but potentially vital genes, can disappear from these rapidly selected populations making further adaptation to new stressors, such as diseases found in an unpolluted environment or a new chemical, more difficult or impossible.
In another form of chemical induced genetic damage, useful genes can be mutated into useless genes or even harmful genes. Cancer is a common endpoint of chemical mutagen activity in body (somatic) cells. Gene mutations can also seriously impair the function of somatic cells such as blood lymphocytes that protect the body from bacterial infections. In the germ cells (i.e. sperm and egg cells), mutations can produce direct permanent changes that are passed from the individual to the general population in future generations. Guttman and his colleagues at Miami University showed that deformities in fluoranthene exposed flat head minnows was a result of mutagenic damage in the sex (germ) cells. In addition, Hedenskog and colleagues at Stockholm University demonstrated minisatellite gene mutations in male mouse germ cells after animals were exposed to polychlorinated biphenyls (PCBs) and low levels of diesel exhaust. The mutations were transmitted to offspring produced from mating with unexposed females. Thus this mutation has become a permanent feature in this breeding line of mice. In humans, mutations in other mini-satellite regions can increase the risk of diseases such as cancer and diabetes.
Germ cell mutations, even if harmful and selected against, will likely remain in the population for many generations. Thus in an environment of a chemically induced increase in the background mutation rate, there will be an increasing legacy of useless or harmful genetic material that is created within each generation by an ever increasing build-up of genetically toxic chemicals. These effects may be compounded each generation. Under unpolluted conditions, natural mutation events are slowly accumulated and form a reservoir of material (genetic load) for evolutionary change. At high levels, this mutational load becomes a drag on the population and can result in an enormous burden of useless mutated genes resulting in greater embryo and pre-reproductive mortality. At lower levels, the genetic flexibility of the population is diminished.
The repercussions in the reduction of general genetic variation is especially serious when populations face novel environmental stresses. For example, new man-made chemicals, a new disease or a relatively sudden climatic shift (such as global warming), increased UVb rays reaching the earth though holes in the ozone layer and other phenomena will require genetic changes in populations to ensure survival of the species. Adaptation has been further restricted by fractionation of species ranges as a consequence of habitat destruction through forestry, agriculture, mining and urbanization. This habitat isolation has severely reduced the potential for vital genes to flow through the entire species range and maximize the possibility of adaptation. If the population is unable to genetically respond effectively, extinction is then likely.
Ultimately our environment is becoming more and more genetically toxic as the volume and variety of man-made chemicals increases each year. Like water running through our fingers, we cannot stop the evolutionary pathways of many species from being directed by endemic man-made chemicals. Future genetic stresses may well push many of these genetically weakened species to extinction. In 1989, Miller and his colleagues wrote in the journal Fisheries an article outlining the extinction of fish species over the past 100 years. They found that of the 3 genera, 27 species and 13 subspecies of fish that have totally disappeared from our planet, chemicals and pollutants were a contributing factor in 38% of the cases. At present, we have no idea how many species are at immediate risk from genetic damage. In the few instances where we have done the field research, usually in regions of heavy pollution, we have found both evidence of genetic damage and evidence of changes in gene frequencies within those populations. For example, Murdoch and Hebert showed that brown bullheads in the Great Lakes from pristine areas had much higher genetic diversity than bullheads from sites contaminated with organochlorines and petrochemicals.
How are the regulators dealing with the problems and issues being discovered with an ever increasing frequency in this new field of ecological genetic toxicology? At the present time the regulations covering the monitoring of our environment in the United States, Canada and elsewhere rely almost totally on the endpoint effect of death in fish over the span of a 96 hour exposure to a particular dilution of a chemical or effluent. For example in British Columbia, enough fish routinely survive the 96 hour exposure to 100% effluent from bleached Kraft pulp mills with modern secondary treatment that the effluent is frequently termed non-toxic. I and my colleagues have recently shown, this effluent is highly genotoxic to fish at concentrations ranging from 2% to 16%. We have not yet identified the no effect concentration. The effects of chemical management in agriculture has again come under scrutiny with the work of Lowcock and his colleagues from Quebec who examined DNA damage in the green frog populations in that province. Field studies showed that frog populations found in ponds receiving surface runoff from nearby potato and corn fields exhibited significant DNA damage and growth deformities compared to frog populations in non-agricultural areas. Frogs are particularly susceptible to the effects of agricultural chemicals because of their amphibious life-style and semi-permeable skin.
Thousands of new manufactured chemicals are introduced as either products or effluents into our environment each year. Most have not been adequately tested prior to release. Absolutely no consideration is given to the regular monitoring of and testing for the genetic effects of these chemical products to the plant and animal populations in our environment. Where such effects have been clearly shown, federal governments have yet to effectively respond with either sufficient funds for additional research, or appropriate new regulations (not guidelines!!) or enforcement of existing regulations. Inaction could be viewed as a significant subsidy to industry and could have implications for litigation, especially for Directors. For example, the tobacco industry is now paying some portion of the genetic cost of its products which release many mutagens into the environment some of which in humans cause premature death through cancer and other diseases. Many more species other than our own are being affected by the industrial chemicals in the air and water and some will endure the ultimate consequence of extinction.
What is the value of a species? What is the cost for the loss of one gene to a population?
The field of ecological genetic toxicology is in its infancy and requires significant financial support for more research in order to define the immensity of the problem that we are faced with today and for the foreseeable future. We have the means to enable us to find out the degree of damage in any population and how this damage is impacting the genetic fitness of the population. We just need the financial resources to get on with the work. Traditional government funding sources are no longer available owing to the fiscal deficit restraint program. But can we afford to ignore for another moment the genetic debt that is building ever greater? The end of many species, possibly including man, could come about not from the catastrophic effects of atomic bombs, but from the genetically damaging effects of our toxic urban environment, short-sighted industrial practices and the ineffectiveness and inadequacy of present government regulations to reduce the rate of an ever increasing debt of genetic damage. Unlike the fiscal debt, the genetic damage debt cannot be paid off.
The author is a Canadian geneticist who
researches the genetic effects of pollution in natural