“A comparison of a normal Atlantic killifish embryo, left, and an embryo affected by a group of chemicals called PCBs. The fish on the right has a deformed heart. Killifish that have evolved tolerance to chemical exposure show signs of developmental defects.”
SUB-LETHAL METABOLIC EFFECTS
Fish DNA can change in response to pollution
by Anna Robuck / October 4, 2017
“Unless you live in a bubble, you are full of contaminants. Somewhat unreassuring news: every other living creature on Earth seems to share this condition with you. Both terrifying and unifying, widespread contamination in humans and wildlife arises due to the slow and constant accumulation of chemicals in living creatures from their surrounding environment and diet, in a pathway known as bioaccumulation.
Virtually everything you or any other living creature do contributes to this buildup: consumer products, food, textiles, building materials, household dust, drinking water, surface water, deep water, soil, and even air have all been found to contain multitudes of human-created chemicals. A recent study has even found microplastic fibers in municipal drinking water supplies across the country and globe. Despite our chemical-laden lifestyles, we have almost no comprehensive idea how the accumulation of these compounds impacts living creatures, particularly wildlife, beyond acute effects. Yes, some chemicals have been shown to cause cancer or seriously mess up hormone production in humans or wildlife. But most chemicals in the environment primarily act by changing or weakening organisms’ overall health in ways that don’t outright kill them.
This poor understanding stems from the fact that it is difficult to pin down definitive or causal relationships between pollution and its consequences when so many other factors could be at play in complex living systems. When a human gets cancer or a bird is having trouble laying eggs, it is nearly impossible to parse out how contaminants contributed in conjunction with variables like age, genetic inclination, nutritional state, and other environmental stressors. Yet the challenging nature of the problem hasn’t dissuaded researchers from broaching it, and we are slowly starting to better understand how contaminants impact living beings.
“The Elizabeth River (ER) Superfund site represents a “natural-experiment” to explore this hypothesis in several subpopulations of Atlantic killifish that have evolved a gradation of resistance to a ubiquitous pollutant—polycyclic aromatic hydrocarbons (PAH).”
One recent study in particular helps highlight just how far we’ve come in understanding the sub-lethal metabolic effects contaminants have on wildlife. The international team, led by Nishad Jayasundara of the University of Maine at Orono, focused on the mummichog, a common and well-studied fish that primarily lives in estuaries, marshes, and coastal environments. Mummichogs have long demonstrated a unique ability to adapt to polluted environments, with various lab and field research documenting genetic and physical adaptions to a variety of contaminants like heavy metals, pesticides, and other organic chemicals.
The team built upon this prior research by taking advantage of a natural experiment ongoing in the Elizabeth River along the coast of Virginia. Mummichog populations in the Elizabeth inhabit differently contaminated sub-environments within the larger river system. The team collected live fish from sites known to contain high, medium, and low levels of polyaromatic hydrocarbons (PAHs), a toxic and carcinogenic pollutant. The fish were then allowed to acclimate to environmental conditions in captivity before undergoing comprehensive evaluation.
After the acclimation period, the researchers first focused on genetics, and used previously existing work to identify genes that are different in contaminated and uncontaminated fish. They specifically looked at genes related to metabolism. From there, it was time for fish “Olympics.” The researchers made the fish swim until tired while measuring their oxygen consumption, metabolic rate, swimming ability, and tolerance to increased temperatures. The results of these measurements were fed into a statistical model to extrapolate how differential fish physical fitness impacts how the fish moves and responds within its environment.
Using this multi-tiered strategy, the researchers described how pollution had cumulative effects at the levels of DNA, animal, and ecosystem. They found something surprising. Mummichogs deal with PAH exposure by changing their gene makeup. Let that sink in a minute: fish DNA actually changes to cope with polluted environments. This alters metabolism and energy allocation, thereby compromising the fish’s ability to deal with other stressors in their environment. In this study, fish from polluted environments were less able to cope with increased temperatures; this has huge implications in a warming world where climate change is at work to increase water temperatures around the globe.
This is also troubling because mummichogs are considered extremely habitat-flexible, dealing with wide ranges in temperature and salinity. If any creature should be able to cope with thermal stress, it’s these guys. Additionally, the modeling work suggested the compounded effects of altered genes, metabolism, and coping ability translates to fish being less capable of finding and traveling to an optimum environment, meaning contaminant exposure has the potential to alter the very way fish interact with the surrounding environment. But what about all the wildlife that’s bigger than the size of a finger? How do contaminants sublethally impact cats, pigs, sharks, weasels, deer, or seabirds? Unfortunately, when larger creatures are factored into the conversation, we are reminded that we understand little when it comes to sublethal impacts of contaminants in wildlife.
A recent study focusing on Arctic seabirds embodies such existing gaps and highlights how tough it is to figure out how contaminants are undermining wildlife processes and function. Few studies have tackled contaminant impacts on metabolism in birds, thanks to how hard it is to compare features of very different species, as well as the fact that studying live creatures in the wild is much harder than analyzing samples. Those that have forged ahead looking at bird hormone production and metabolism have seen conflicting results.
So there is scant consensus regarding how birds metabolically respond to contaminant burdens. An international team led by biologist Pierre Blévin, of the Centre d’Etudes Biologiques de Chizé in France, recognized this uncertainty and implemented a study in an effort to better understand how contaminants are related to energy use in live birds. The team captured black-legged kittiwakes, a type of Arctic seabird, during their chick rearing season on Svalbard in Norway and took blood samples from captured birds for contaminant and hormone analysis. The birds were then rushed back to the lab via boat to take respirometry measurements. Respirometry essentially measures carbon dioxide respiration and oxygen consumption over time, allowing calculation of metabolic rate.
Unfortunately, no clear picture emerged. The researchers found that different groups of contaminants were associated with variable metabolic rate and hormone levels. Increased concentrations of banned chlorine-based compounds, like pesticides or PCBs, were associated with decreased metabolic rate and hormone levels, while currently used perfluorinated chemicals, used as water repellants, were associated with an increased metabolic rate only in females. These inconsistent results provide more questions than answers in terms of parsing out the greater impact of contaminants on birds. If organochlorine and perfluorinated compounds have opposite effects on metabolism, does this mean they cancel each other out? What is the net effect on bird energy use and what does this mean for bird migration? These birds migrate thousands of miles; do contaminant metabolic artifacts impact these feats?
It’s hard to say: wild animals that live longer lives come with a history full on unknown events that may easily confound snapshots of metabolic rate or contaminant signature obtained within a study. In terms of methodology, transporting large wild animals alive for metabolism measurements is extremely time-consuming, expensive, and location-dependent, not to mention a permitting nightmare depending on the study location. This contrasts starkly with research solely measuring contaminant body burdens, which just uses tissue from dead animals. This is exponentially more straightforward, and cheaper, hence the abundance of reports describing contaminant levels in animals with little indication of how found chemicals are impacting the animal or its day to day function.”
UNNATURAL LABORATORIES : HUMAN-INDUCED EVOLUTION
Some animals are adapting to pollutants in surprising and costly ways
by Brittney Borowiec / November 16, 2017
“No other species pollutes the way humans do. Many pollutants, like dioxins, phenyls, hydrocarbons, and some pesticides, are so slow to degrade that they can persist for generations in an environment. Others, like the caffeine and birth control hormones we flush down the toilet daily, are released so constantly that they are replaced as rapidly as they are broken down. Animals are doing their best to weather this hurricane that humanity is wreaking on the natural world. Some, like pigeons and rats, seem to thrive in new urban environments. Others, like coral reefs and giant pandas, seem to be dangerously close to extinction. Animals that are best able to cope with human-caused climate shifts tend to be the ones to pass on their genes to the next generation. In this way, these selective pressures are the rules by which the “winners” and “losers” are decided, and influence the building blocks (genes) of evolution in a species. We don’t know for certain how this will play out in animal populations around the world, but one place scientists are looking for clues is within lineages that have survived for a long time already in difficult environments, both natural and human-induced.
They have found that animals can adapt to polluted environments, and persist even in environments that are inhospitable to most living things, but that those changes cause evolutionary trade-offs. The ideal solution for one problem (like pollution) can lead to terrible consequences in another process (like reproductive success). This means that even if animals are able to initially survive in polluted environments, they’ll still have to contend with long-term consequences that are difficult to predict, and could ultimately lead to their decline. And species that are able to escape extinction, and even thrive, like urban rats, are going to be drastically different from ancestors that evolved without human influence. Last month, researchers from Kansas State University and Juárez Autonomous University of Tabasco, in Mexico, reinforced this finding by examining how life in a toxic spring shaped the multiple independent evolutionary lineages at the site.
The Poecilia mexicana species complex is composed of multiple independent lineages of fish that have colonized toxic, hydrogen sulfide-rich springs occurring naturally in river drainages in southern Mexico. Fish from sulfuric springs show a suite of behavioral, physiological, and anatomical differences from populations in nearby, non-sulfuric springs. While the hydrogen sulfide in these springs is the product of a nearby volcano, it can also make its way into the aquatic environment from petroleum refineries, paper mills, and sewage. Because the populations in sulfuric and non-sulfuric springs are isolated from each other and have continued on their evolutionary trajectories independently for some time, they form a fascinating natural laboratory that scientists can use to ask questions about how animals adapt to extreme environments.
Hydrogen sulfide is a respiratory toxicant — it shorts out mitochondria (“the powerhouse of the cell”) and makes energy production slow and inefficient. This is exacerbated by the fact that it takes a lot of energy — dedicated proteins and metabolic processes — to detoxify hydrogen sulfide to reasonable levels. Contributing to this chronic energy shortage is that few lifeforms can survive in the extreme conditions of the springs, meaning that food for predators like fish is limited. Given this energy shortage at multiple levels of biology, the researchers hypothesized that perhaps populations from hydrogen sulfide-contaminated springs adapted to have lower energetic demands than fish from uncontaminated waters. By saving energy on routine maintenance, they reasoned, the fish would be able to allocate more of their limited energy stores to non-survival functions like reproduction.
The team surveyed the body size and routine metabolic rate, two indicators of whole-animal energy demands, of Poecilia fishes from 11 field sites (five sulfuric and six non-sulfuric). They also reared fish from a subset of sites in the lab and conducted the same analyses. This extra step allowed them to track down whether any differences observed between the populations had a genetic basis (since they would remain even after the fish were raised in the same environment). In support of their hypothesis, fish from sulfurous springs showed evidence of adaptation for lower energetic demands — they were smaller, and had lower oxygen consumption rates than fish from uncontaminated sites, even when reared in the lab. Though some river drainages showed more pronounced differences between sulfuric and non-sulfuric populations, there appeared to be convergent evolution for lower energetic demands in the Poecilia fishes, as multiple, distantly related, independent lineages appeared to find the same solution to the problem of life in a toxic spring.
Like the fish confined to hydrogen sulfide-rich springs, killifish from a number of polluted sites have made similar adjustments in their physiology to adapt to their extreme environment. The species, which holds a special place in my heart, are renowned for their remarkable tolerance of a wide swath of environmental challenges including low oxygen, high salinity, large swings in temperature, and even the microgravity of space. They also have a reputation for being one of the few species that will doggedly persist in sites besieged by contamination, and have been the subject of intensive toxicological research.
This all makes them a model ripe for examining how animals are rapidly adapting to our increasingly polluted world, and intensive study of the genetics and physiology of killifish populations residing in densely populated, urban estuaries on the Atlantic coast has taught us a lot about the population-level effects of pollution. Compared to animals from clean sites, killifish from polluted areas are far more tolerant of a large class of persistent, toxic compounds like polyaromatic hydrocarbons (PAHs), polychlorinated biphenyl (PCBs), and dioxins. And in spite of huge site-to-site variation in the exact nature of the toxic soup, the fish all seem to have the same basic adaption: desensitization of the aryl-hydrocarbon receptor pathway, an important detoxifying pathway that allows proteins to break down the toxic compounds that would otherwise harm them.
But why shut down a cellular response that helps to break down pollutants? The working theory is that desensitizing that pathway avoids its over-activation in contaminated sites, which can disrupt normal cell processes and lead to cell death. More focused work on specific populations has shown that these changes evolved quickly, repeatedly, and independently. Conceptually, the sulfur-rich springs of southern Mexico are not all that different from a polluted killifish environment or a highly contaminated superfund site, where animals are persistently exposed to a cocktail of nasty urban and industrial chemical by-products. As animals come to grips with the new reality of life on Earth with humans, evolution marches on, as has been the case for thousands and thousands of lineages over millions of years. Only now, it’s a race to adapt to what we’re doing to the planet. Humans are the world’s greatest evolutionary force. How will animals cope with the new reality of polluted habitats? We can look at lineages that have survived for a long time in difficult environments (both natural and human-induced) for clues.”
PRE-POLLUTED at BIRTH
NO WONDER (EVERYBODY’S CRAZY)