In a paper titled “Use Antimicrobials Wisely,” published in the current edition of Nature, a nine-member international research team, including Carroll, advocates that the United Nations reframe its action on antimicrobial resistance.
The United Nations is meeting in New York on Sept. 21 to discuss the global antimicrobial drug resistance (AMR) crisis.
“We're concerned about what will happen if the proposed UN solutions focus mainly on incentives for new drug development, at a time when the drug industry itself is abandoning those efforts against infectious disease due to AMR,” said Carroll, who co-leads the international group on resistance to pesticides and antimicrobial drugs. He founded and directs the Institute for Contemporary Evolution, Davis, and is a member of the Sharon Lawler lab, UC Davis Department of Entomology and Nematology.
The paper, published in the Comment section, is the first product from a two-year working group sponsored by the National Socio-Environmental Synthesis Center in Annapolis, Maryland. “We are taking a similar socio-environmental approach in our concurrent work on pesticide stewardship,” Carroll said.
“While new drugs have a role, we think it's more important for society to learn how to steward pathogen susceptibility, so we develop that theme in the paper,” Carroll said. “And because we also depend on microbes for digestion, immunity, and general health, and microbes support ecosystem functioning through nutrient cycles and the maintenance of soil and water quality, we further argue that our AM drug habits and waste streams threaten both personal and planetary health. “
Lead authors of the paper are Peter Jorgensen of Stockholm, Sweden, and Didier Wernli of Geneva Switzerland. Jørgensen, who spent part of his Danish graduate program working with Carroll in Davis, is now a postdoctoral researcher at the Royal Swedish Academy of Science, Stockholm.
Carroll described AMR as more than a medical dilemma—it's a socio-ecological problem. “The vulnerability of pathogens to antimicrobial drugs is a communal resource, readily threatened by overuse, to be lost as a classic 'tragedy of the commons.' There is a lot of contemporary theory for social resilience in the face of socio-ecological challenges, and– linking to entomology– the early success of the pioneering management of Bt crop pest resistance evolution is an encouraging precedent.”
In its planetary health approach, the group seeks to be “more cognizant not only of preserving drug susceptibility in pathogenic microbes, but also protecting from wholesale destruction the community of microbes on which we depend for life,” Carroll said.
In the paper, the scientists pointed out that “Resistance affects animal and environmental health as well as human health, and so requires coordinated action across economic sectors. No single concern exemplifies this better than the high rate of antibiotic use in agriculture (largely as growth promoters or disease prevention).” They wrote that in the United States, 70 to 80 percent of all anti-microbials consumed are given to livestock.”
Now newly published UC Davis research shows that soapberry bugs have not only lost adaptations to their native host plant but are regionally specializing on an invasive host.
The work, "Adaptation to an Invasive Host Is Driving the Loss of a Native Ecotype," published in the current edition of the journal Evolution, “collapses a classic and well-documented example of local adaptation,” said doctoral candidate Meredith Cenzer of the Louie Yang lab, UC Davis Department of Entomology and Nematology. The plant-host switch can lead to disruption of native plant communities and a breakdown of the ecosystem.
The players involved are the soapberry bug (Jadera haematoloma), also known as “the red-shouldered bug”; its native host plant, the balloon vine (Cardiospermum corindum), and the invasive host, the golden rain tree or Taiwanese rain tree (Koelreuteria elegans).
The study, which took place in Florida, expands on the 1989 groundbreaking research of UC Davis evolutionary ecologist and soapberry expert Scott Carroll, who documented local adaptation in beak length, survival, and development time and other traits between soapberry bugs, balloon vine and the golden rain tree in Florida.
Said Carroll: "Meredith Cenzer's findings carry an important message for those concerned with biodiversity conservation, because she shows that even highly distinct adaptive specializations can disappear rapidly due to human influence on the environment– even in cases where the key native habitat has not been lost."
The soapberry bug, which lives throughout the United States and much of the world, feeds on seeds within the soapberry plant family, Sapindaceae, which includes soapberries, boxelders and maples. Mostly black, it has red eyes, red lateral stripes on the sides of its head and red on its “shoulders” (pronotum). It is often mistaken for the boxelder bug.
“As part of my doctoral dissertation, I documented that this pattern of local adaptation has been lost in the last 27 years,” Cenzer said, “and that all populations of soapberry bugs in Florida-- even those still found on the native --are now adapted only to the invasive host.“
“Locally adapted populations are often used as model systems for the early stages of rccological speciation, but most of these young divergent populations will never become complete species,” Cenzer noted in her abstract. “The maintenance of locally adapted populations relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments.”
“All populations that were adapted to the native host--including those still found on that host today--are now better adapted to the invasive host in multiple phenotypes,” she wrote in her abstract.” Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.”
Cenzer characterized local adaptation as “high performance in one habitat coming at the cost of performance in other habitat types, such that populations specialized on each habitat will have higher fitness in that environment than immigrants from other habitats.”
“This results directly in two types of ecological reproductive isolation between locally adapted populations: 1) selection against migrants, who will be outcompeted by residents, and 2) selection against hybridization (if hybrids show intermediate phenotypes), as hybrid offspring will be outcompeted in each habitat by one parental type,” she wrote in her research paper. “However, such reproductive isolation relies on ongoing differential selection balanced with low rates of gene flow between habitats. In most well studied systems demonstrating local adaptation, we do not know how perturbation – either to selection pressures or gene flow – will influence the long-term stability of differentiation.”
Carroll, who maintains a website, “Soapberries of the World,” says the soapberry bugs are “very approachable native guides to how evolution is taking place on earth day.” His website shows “how evolution happens every day and why it matters.”
A native of Gainesville, Fla., Cenzer received her bachelor of science degree in entomology at the University of Florida in 2009.
“I am broadly interested in evolutionary ecology, particularly in plant-insect interactions, and the balancing roles of selection, gene flow, and plasticity on determining the phenotypes we see in nature,” she said. After receiving her doctorate in entomology from UC Davis in the fall, she will start a postdoctoral position at Florida State University with biology professor Leithen M'Gonigle, developing theory on the evolution of dispersal in patchy landscapes.
"Two categories of evolutionary challenges result from escalating human impacts on the planet," Carroll says. "The first arises from cancers, pathogens and pests evolving too quickly, and the second from the inability of many valued species to adapt quickly enough."
Carroll says that applied evolutionary biology offers strategies to address these global challenges that threaten human health, food security and biodiversity and natural resources.
He will highlight both progress and gaps in evolutionary methods across the life sciences that either "target the rate and director of evolution or reduce the mismatch between organisms and human-altered environments."
"Refining and applying these underused tools will be vial for meeting current and future targets for sustainable development."
Carroll does research on patterns of ongoing evolution in wild and anthropogenic environments. He is well-known for his studies on evolutionary changes in soapberry bugs in response to plant introductions. His expertise includes behavioral and evolutionary aspects of adaptation to contemporary environmental change in insects and other organisms.
See latest research on evolutionary biology techniques
See Science Express: http://www.sciencemag.org/content/early/2014/09/10/science.1245993.full.pdf
The paper appears in the Sept. 11 in Science Express, which makes important papers available to readers before they appear in the journal Science. The first-of-its-kind study will appear in a November edition of the journal.
“Evolutionary biology is often overlooked in the study of global challenges,” said lead author Scott Carroll of the UC Davis Department of Entomology and Nematology and the Institute for Contemporary Evolution, also in Davis. “By looking at humanity's problems across the domains of nature conservation, food production and human health, it is clear that we need to strengthen evolutionary biology throughout the disciplines and develop a shared language among them.”
The study, “Applying Evolutionary Biology to Address Global Challenges,” calls attention to how evolutionary biology techniques can be used to address challenges in agriculture, medicine and environmental sciences, said Carroll, noting that these techniques, although seemingly unrelated, work within a similar set of evolutionary processes.
“These techniques range from limiting the use of antibiotics to avoid resistant bacteria and breeding crops with desired benefits such as flood tolerant rice, to less commonly implemented strategies such as gene therapy to treat human disease, and planting non-native plants to anticipate climate change,” Carroll said.
“A particular worry is the unaddressed need for management of evolution that spans multiple sectors, such as occurs in the spread of new infectious diseases and antimicrobial resistance genes between natural, human health and agricultural systems.”
Co-lead researcher and biologist Peter Søgaard Jørgensen of the University of Copenhagen, Denmark, agrees. “Many of the global challenges we face today have common biological solutions,” he said, “but we can tackle them effectively only if we are aware of successes and progress in all fields using evolutionary biology as a tool.”
In their paper, the nine researchers—two from UC Davis, one from UCLA and six from universities in Denmark, New Zealand, Maine, Minnesota, Washington state and Arizona--crafted a graphic wheel divided into three sectors, food, health and environment and cited the challenges that link them together, including rapid revolution and phenotype environment mismatch in more slowly reproducing or threatened species.
Carroll said the underlying causes of societal challenges such as food security, emerging disease and biodiversity loss “have more in common than we think.”
“Humans, pathogens and all other life on earth adapt to their environment through evolution, but some adaptation happens too quickly and some too slowly to benefit human society,” Carroll said. “Current efforts to overcome societal challenges are likely only to create larger problems if evolutionary biology is not swiftly and widely implementedto achieve sustainable development.”
Society faces two sorts of challenges from evolution, the research team said. “The first occurs when pests and pathogens we try to kill or control persist or even prosper because the survivors and their offspring can resist our actions,” Carroll said. “The second challenge arises when species we value adapt too slowly, including humans.”
Although practices in health, agriculture and environmental conservation differ, each field can better target challenges using the same applications of evolutionary biology, they said.
For example, when a farmer plants a crop that is susceptible to pests, he might actually help the agricultural community as a whole by slowing down evolution of pesticide resistance, the authors said, citing an applied evolutionary biology tactic used in agriculture.
Planting pest-friendly crops has been used in the United States with good results, the team said. Farmers planting these crops slow the evolution of resistance to genetically modified corn and other crops. Pests then reproduce in abundance eating the susceptible plants, and when a rare resistant mutant matures on a toxic diet, it is most likely to mate with a susceptible partner, keeping susceptibility alive. This approach works to suppress the unwanted evolution on the whole, but farmers will have sacrificed a short-term gain for the long-term good.
Similar innovative solutions exist across the fields of medicine and environmental conservation, they said.
“This is an example of how implementing applied evolutionary biology without a plan for regulatory measures may come at short-term costs to some individuals that others may avoid.” Jorgensen said. “By using regulatory tools, decision makers such as local communities and governments play a crucial role in ensuring that everybody gains from the benefits of using evolutionary biology to realize the long-term goals of increasing food security, protecting biodiversity and improving human health and well-being.”
Other co-authors are Michael T. Kinnison, University of Maine; Carl Bergstrom, University of Washington; R. Ford Denison, University of Minnesota; Peter Gluckman, University of Auckland, New Zealand; Thomas B. Smith, UCLA; Sharon Strauss, UC Davis Department of Evolution and Ecology and Center for Population Biology, and Bruce Tabashnik, University of Arizona.
Carroll is an affiliate of the Sharon Lawler lab, UC Davis Entomology and Nematology. The research was funded in part by the National Science Foundation and the Australian-American Fulbright Commission.
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To celebrate the 25th anniversary of the journal, published by the International Society for Behavior Ecology, the editors chose the most influential articles and reviews, and compiled them in a celebratory Virtual Issue.
Carroll's paper on the ecology and genetics of adaptive differences among soapberry bug populations in the plasticity of mating behavior, was not only selected as the most influential paper, but his photograph of the bugs at his study site, the Florida Keys, graced the cover.
Editor-in-chief Leigh Simmons of the Center for Evolutionary Biology, University of Western Australia, described Carroll's work as "a beautiful study of divergence in phenotypic plasticity in mate guarding in these creatures."
The research paper is titled Divergence in Male Mating Tactics between Two Populations of the Soapberry Bug: II. Genetic Change and the Evolution of a Plastic Reaction Norm in a Variable Social Environment.
Carroll conducted the research as part of his dissertation at the University of Utah, under professor Eric Charnov. He co-authored the paper while a post-doctoral scholar in the laboratory of Hugh Dingle, UC Davis Department of Entomology (now the Department of Entomology and Nematology). His co-author, Patrice Corneli, now an associate research professor in the Department of Biology, University of Utah, analyzed aspects of the data for her master's thesis in statistics, also awarded at the University of Utah.
As the director of the Institute for Contemporary Evolution, Carroll does research on patterns of ongoing evolution in wild and anthropogenic environments. His studies on evolutionary changes in soapberry bugs in response to plant introductions are seminal contributions to our understanding of diversification.
The UC Davis evolutionary ecologist is the co-editor of the book, Conservation Biology: Evolution in Action (Oxford University Press, 2008) with Charles Fox, professor of insect genetics, behavior and evolutionary ecology, University of Kentucky.
Highly recognized for his work, Carroll co-authored a research paper that was selected in 2013 as one of the top 100 most influential papers ever published in the worldwide British Ecological Society, headquartered in London. The 13-page article, “Adaptive Versus Non-Adaptive Phenotypic Plasticity and the Potential for Contemporary Adaptation in New Environments,” was published in April 2007 (Volume 21) in the society's journal, Functional Ecology.
Scott received his bachelor's degree in ecology and behavioral ecology, magna cum laude, from the University of Minnesota in 1981, and then went on the earn his maser's degree in zoology, with distinction, from the University of Oklahoma in 1983 before receiving his doctorate in biology in 1990 from the University of Utah.