Life will find a way: a story from chemical ecology...and 2017?

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2016 was a doozy. Merriam-Webster Dictionary nailed it when they named "surreal" the word of the year. That's because so many unexpected, upsetting and very serious events transpired in the past 12 months. Events that left us, at the very, very least, dazed and confused and wondering, when will this year end again?

So if you are are looking for some last-minute inspiration to carry you from the Year of the Crazy into 2017, Year of the ?, then you have come to the right place. Today I am here to provide an encouraging and optimistic note from the land of chemical ecology: As we've seen time and time again on our blog, life will find a way!

An article published in the New York Times on December 9th highlighted recent research that touches on common themes in chemical ecology. The research was published in the journal Science and is entitled "The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish." This work was a collaborative effort by scientists from the University of California Davis, the Woods Hole Oceanographic institute, and several other universities/institutes. The paper focuses on the question, how do organisms adapt to high levels of pollutants that humans have dumped into their ecosystem? How does a pollutant-sensitive organism become resistant to these toxic chemicals?

The researchers asked these questions in the context of Atlantic killifish populations, which, in certain geographic areas off the coast of the Northeast, have adapted to levels of halogenated aryl hydrocarbons and other persistent industrial chemicals that would normally be lethal to these fish. The questions posed by this paper are important to consider as many populations of animals throughout the world are in decline due to the activities of humans. The human-generated pollutants, often highly toxic to animals, have introduced new, strong selective pressures on organisms. Can we predict which organisms may be better equipped to adapt to these selective pressures by looking at the genetics of populations that have successfully evolved to live in polluted spaces?

Chemical pollutants are not created equal. Each chemical can impact health through different mechanisms, and that toxicity can be caused by widely different dosages. Chemicals even have very different stabilities-- some stick around environment for decades while others are degraded quickly. The same molecule can even impact organisms at different trophic levels (a trophic level indicates where in the food chain of a particular ecosystem an organism lives, from the large predators in an ecosystem, to the herbivores, plants and finally the bacteria at the bottom of the food chain) in different ways. Take, for instance, the case of neonicotinoids: these highly used pesticides effectively kill insects, of course, and can also impact the health of bird populations that rely on the bugs for their food.

The Atlantic salt-marsh estuaries where the Atlantic killifish (Fundulus heteroclitus) makes its home are polluted with a cocktail of persistent industrial chemicals including halogenated aryl hydrocarbons like the infamous polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs). These pollutants bioaccumulate, meaning that fish and other animals that live in contaminated waters will accumulate the molecules in their tissues, much like mercury and tuna. PCBs affect fish growth at the embryo stage: susceptible fish do not develop normal tissues or organs and often do not survive to adulthood.

To ask the question, what genetic changes happened that allowed populations of Killifish to thrive in polluted waters, the researchers collected fish from eight sites, both contaminated and pristine (each contaminated site was paired with a nearby pristine site), where the killifish were either tolerant or susceptible to pollutants, respectively. One of the most contaminated sites is at New Bedford, Massachusetts, a so-called "Superfund site" where PCBs were discharged into the waters as industrial wastes for thirty years. The genomes of 50 fish from each of the sites were sequenced. First, the researchers found that the populations that were closest geographically had the most similar genetic backgrounds, and from this data they concluded that tolerant fish populations evolved independently. In other words, there was not one group of fish that evolved to be tolerant and then spread out to the other sites, but rather evolution happened at each of these sites independently.  

Next, the researchers analyzed the genomic data of the pairs of tolerant/susceptible groups of fish and looked for regions in the genomes with particularly high nucleotide diversity between the two groups; these outlier regions could give clues as to what gene changes differentiate tolerant from susceptible relatives. They found several genetic loci that were different across the four pairs of tolerant/susceptible groups. However there was a set of genes that was shared among the geographically separated tolerant populations and looked to be under strong selection. The genes are all involved in how the fish responds to aryl hydrocarbons, namely genes in the aryl hydrocarbon receptor pathway.

To follow up on these nucleotide changes shared by the tolerant fishes, the researchers measured the amount that these genes were expressed when the fish were raised for two generations in a clean environment and the embryos from the second generation were challenged with a PCB. They found that expression of genes in the aryl hydrocarbon receptor pathway was much lower in the fish derived from the tolerant populations than those from the susceptible populations. In essence, the fish that are tolerant to PCBs have become desensitized to these chemicals. From these results, the researchers conclude the aryl hydrocarbon receptor "signaling pathway is likely a key and repeated target of natural selection in tolerant populations."

From this work, we see that killifish from various polluted sites have undergone convergent evolution in order to adapt to ecosystem contamination. The killifish have converged on a solution to toxicity that involves dampening the cell's response to the presence of PCBs and related compounds. Essentially,  toxicity is mediated by decreasing the expression of genes that encode for the proteins that change cellular gene expression in response to PCBs.

A central question that follows from this work is, can we expect other populations to respond in the same manner as the killifish or are these common fish somehow special in their ability to adapt to a toxic environment? In the Science paper, the authors state that "selection on preexisting variants was important for rapid adaptation in killifish and that multiple molecule targets were available for selective targeting of a common pathway." The translation of this important concluding statement has two parts.

First, killifish may have been particularly successful at evolving to withstand pollutants because the killifish population was large and genetically diverse from the get-go. A larger population means there's a higher probability that an individual within that group has a mutation that lends it greater reproductive success in the face of a evolutionary pressure (in this case, toxic chemicals).

The second part of this concluding statement is also important and gets back to the "chemicals are not created equal" line of thought expressed above. For PCBs, the pathway in the cell that translates reception of the chemical signal into changes in gene expression involves many proteins. The moving parts of the PCB response in the cell means there are multiple targets in the pathway for evolutionary change. The authors suggest that because there are multiple proteins required for this pathway to function there are more chances for nucleotide changes to impact the cell's response to the chemicals. In contrast, if there was just one gene involved in responding to PCBs, there is a lower probability that a genetic variant in a population would be a variant in that one gene.

So, to wrap it up: the killifish have survived lethal levels of PCBs to swim another day. And while we should make efforts to clean up our messes when we make them, its encouraging, at least to me, to know that nature finds a way to make it work. Here's to making it work in 2017!

-CAB