Pollution and Restoration:

The Evolutionary Perspective

 

 

Pollution as a source of natural Selection

Foundry Cove was a dumping ground for cadmium and nickel hydroxide wastes. About 53 metric tons of waste entered the cove over the period 1953-1979, when battery manufacturing ceased. Amazingly enough, the bottom creatures living in Foundry Cove were not driven to extinction. In fact, it was rather difficult to tell the communities in Foundry Cove from a nearby unpolluted South Cove. What gives?

 

Polluted environments are places where one sees Darwinian evolution in action. We commonly find that plants and animals can live in sites with very severe copper and cadmium pollution and these species are often resistant to one or more metals. But species collected from clean sites often die when placed in these same environments.

 

We found evolution to be powerful in Foundry Cove, especially when we started to work on the small worm Limnodrilus hoffmeisteri, which is an oligochaete worm common throughout the northern hemisphere. A simple experiment demonstrated this very clearly. We took Foundry Cove worms and South Cove worms (living in a clean environment) and exposed them both to Foundry Cove sediment, which was rich in cadmium. The results were clear cut:

 

The Foundry Cove worms survived well and the South Cove worms mostly died. Was this survival of Foundry Cove worms in polluted sediment the result of natural selection? One way to find this out is to raise the worms through a couple of generations in clean sediment, to see if the resistance persists. Here is what we found:

 

This graph compares survival of worms from South Cove, which was clean (control area) with worms taken from Foundry Cove and their grandchildren, raised through two generations in clean sediment. As you can see, the worms living in South Cove had lower survival in high cadmium concentrations relative to the Foundry Cove worms. Also, the Foundry Cove worms were not very different in survival from their grandparents, collected directly from the Cove. This suggested that the trait of resistance was genetic.

We performed selection experiments in the laboratory on populations from South Cove and found that after three generations of selection in cadmium-rich sediment we could get about 2/3 of the survival found in the Foundry Cove worms. Evolution must have been very fast!

We know that when Foundry Cove worms are exposed to metals, their survival is greater than South Cove worms. But here is another interesting fact: If you expose worms to cadmium it turns out that the survival of parents and their offspring are positively correlated. This means that worms with high survival tend to have offspring with high survival. The relationship is so strong that we can conclude that nearly all of the variation we see in survival is due to genetic differences.

Comparison of survival of offspring to average survival of parents, when exposed to cadmium

 

Other evidence suggests that the trait of high survival is explained by one segregating genetic element. That it, the distribution of survival behaves as if one gene, or a closely linked group of genes, is behind the evolution of resistance.

 

The consequences of this evolutionary event were not good for food webs in the marsh. The tolerance of the worms allowed them to take up cadmium and maintain higher cadmium concentrations than the non-evolved worms. This diagram shows the uptake of cadmium by evolved Foundry Cove worms,relative to unevolved South Cove worms, as a function of the cadmium content of the sediment (micrograms of cadmium per gram sediment):

Uptake of cadmium by Foundry Cove and South Cove worms, as a function of cadmium in the sediment (micrograms per gram sediment)

 

 

What is the biochemical mechanism behind the evolved resistance of the Foundry Cove worms? We have only a bit of evidence, but it is very suggestive. We exposed worms to cadmium and then ran cell extracts through a High Performance Liquid Chromatography (HPLC) separation. The extracts had been exposed to a radioactive isotope of cadmium and we used standards of difference molecular mass to determine the mass of fractions that we collected from the HPLC. As you can see below, one peak stands out. This peak corresponds to a cadmium-binding protein that is not yet more characterized than by its estimated molecular mass of 16,000 Daltons. Still, the evidence suggests that the Foundry Cove worms are genetically distinct and can produce much more of this metal-binding protein than the South Cove worms.

 

Separation of proteins and peptides that bind to cadmium. Note strong peak for worms collected directly from Foundry Cove and for offspring raised in clean sediment. There is a peak also for South Cove worms but it is much reduced. Peak corresponds to a protein of a mass of about 16,000 Daltons.

 

The cadmium was found to be in the cytosol in the worms but also was found as granules, concentrated in the chloragog tissue, which surrounds the gut.

This is a cross section of the worm Limnodrilus hoffmeisteri from Foundry Cove (black on lower left is the gut lumen). The white indicates solid cadmium granules in the chloragog tissue.

 

William Wallace and Glenn Lopez investigated the possibility that cadmium might be transferred from the worms to predators. They fed worms with different amounts of cadmium to the grass shrimp Palaemonetes pugio and found that transfer of cadmium was all associated with the cadmium that was in the cytosol, bound to metal-binding proteins. Cadmium in metal granules were relatively insoluble and were not digested and absorbed by the shrimp.

Transfer of cadmium to shrimp, as a function of the cadmium found in the cytosol of the worm Limnodrilus hoffmeisteri.

 

THE CLEANUP AND REVERSE EVOLUTION

 

FOUNDRY COVE was declared a Superfund site and cleaned up in 1994-1995. This involved dredging the marsh and the cove. The sediment was, on average less than 10 micrograms per gram cadmium, instead of the level of thousands of micrograms before the cleanup.This gave us the opportunity to ask: would evolution reverse the process of survival of Foundry Cove worms? We placed worms in high cadmium concentrations and measured the hours until 50 percent of the worms had expired. We found that the Foundry Cove populations converged to the South Cove populations in only 9 years or 9 generations! Today, the Foundry Cove worms are as vulnerable to cadmium as the worms in South Cove.

Survival time of Foundry Cove and South Cove worms over the years since the cleanup. Note that the survival converges in about 2002, nine years after the cleanup.