Scott P. Carroll

Don't judge species on their origins

Conservationists should assess organisms on environmental impact rather than on whether they are natives, argue Mark Davis and 18 other ecologists.

HOST RACE RADIATION IN THE SOAPBERRY BUG: NATURAL HISTORY WITH THE HISTORY

Evolution by natural selection is remarkably well documented in the diversification of soapberry bug populations on their native and recently introduced host plants. In this century, populations of this native seed‐eating insect have colonized three plant species introduced to North America. Each new host differs in fruit size from the native hosts, providing an unplanned experiment in natural selection of the insects beak length. In each of three host shifts, beak length has increased or decreased in the direction predicted from fruit size. Furthermore, museum specimens show historical changes consistent with the host shift scenario inferred from beak length values in contemporary populations. The extent to which beak length evolution has been accompanied by evolution in other body size characters differs between the races, suggesting that the evolution has proceeded differently in each case. In all cases, significant evolution has occurred in as little as 20–50 years (40–150 generations), creating a species‐level mosaic of response to simultaneous directional, diversifying, and normalizing selection.

GENETIC DIFFERENTIATION OF FITNESS-ASSOCIATED TRAITS AMONG RAPIDLY EVOLVING POPULATIONS OF THE SOAPBERRY BUG

In this study we used reciprocal rearing experiments to test the hypothesis that there is a genetic basis for the adaptive differences in host‐use traits among host‐associated soapberry bug populations (described in Carroll and Boyd 1992). These experiments were conducted on two host races from Florida, in which differences in beak length and development were found between natural populations on a native host plant species and those on a recently introduced plant species (colonized mainly post‐1950). Performance was generally superior on the host species from which each lab population originated (i.e., on the “Home” host species): in analysis of variance, there was significant population‐by‐host interaction for size, development time, and growth rate. These results indicate that the population differences in nature are evolved rather than host induced. Increased performance on the introduced host was accompanied by reduced performance on the native host, a pattern that could theoretically promote further differentiation between the host races.

Evolutionary principles and their practical application

Evolutionary principles are now routinely incorporated into medicine and agriculture. Examples include the design of treatments that slow the evolution of resistance by weeds, pests, and pathogens, and the design of breeding programs that maximize crop yield or quality. Evolutionary principles are also increasingly incorporated into conservation biology, natural resource management, and environmental science. Examples include the protection of small and isolated populations from inbreeding depression, the identification of key traits involved in adaptation to climate change, the design of harvesting regimes that minimize unwanted life‐history evolution, and the setting of conservation priorities based on populations, species, or communities that harbor the greatest evolutionary diversity and potential. The adoption of evolutionary principles has proceeded somewhat independently in these different fields, even though the underlying fundamental concepts are the same. We explore these fundamental concepts under four main themes: variation, selection, connectivity, and eco‐evolutionary dynamics. Within each theme, we present several key evolutionary principles and illustrate their use in addressing applied problems. We hope that the resulting primer of evolutionary concepts and their practical utility helps to advance a unified multidisciplinary field of applied evolutionary biology.

Applying evolutionary biology to address global challenges

BACKGROUND Differences among species in their ability to adapt to environmental change threaten biodiversity, human health, food security, and natural resource availability. Pathogens, pests, and cancers often quickly evolve resistance to control measures, whereas crops, livestock, wild species, and human beings often do not adapt fast enough to cope with climate change, habitat loss, toxicants, and lifestyle change. To address these challenges, practices based on evolutionary biology can promote sustainable outcomes via strategic manipulation of genetic, developmental, and environmental factors. Successful strategies effectively slow unwanted evolution and reduce fitness in costly species or improve performance of valued organisms by reducing phenotype-environment mismatch or increasing group productivity. Tactics of applied evolutionary biology range broadly, from common policies that promote public health or preserve habitat for threatened species—but are easily overlooked as having an evolutionary rationale, to the engineering of new genomes. Tactics and tools of applied evolutionary biology. (Top) Evolutionary tactics to address the major societal challenges treated in the present study are shown as a wheel. Challenges in the food, health, and environment sectors are caused by rapid contemporary evolution or, in more slowly reproducing or threatened species, phenotype-environment mismatch. Gene flow and selection agents make challenges in one sector dependent on actions in others. Current progress in implementing tactics of applied evolutionary biology to address challenges varies widely. (Bottom) Many of these tactics use a common toolbox of strategies to prevent unwanted evolution or to reduce fitness in harmful organisms, as well as to reduce mismatch between organisms and human-altered environments or to increase group performance in desired organisms. Each of these strategies uses a combination of manipulations of the organismal genotype, phenotypic plasticity (development), or environmental conditions. ADVANCES The scope and development of current tactics vary widely. In particular, genetic engineering attracts much attention (and controversy) but now is used mainly for traits under simple genetic control. Human gene therapy, which mainly involves more complex controls, has yet to be applied successfully at large scales. In contrast, other methods to alter complex traits are improving. These include artificial selection for drought- and flood-tolerant crops through bioinformatics and application of “life course” approaches in medicine to reduce human metabolic disorders. Successful control of unwanted evolution depends on governance initiatives that address challenges arising from both natural and social factors. Principal among these challenges are (i) global transfer of genes and selection agents; (ii) interlinked evolution across traditional sectors of society (environment, food, and health); and (iii) conflicts between individual and group incentives that threaten regulation of antibiotic use and crop refuges. Evolutionarily informed practices are a newer prospect in some fields and require more systematic research, as well as ethical consideration—for example, in attempts to protect wild species through assisted migration, in the choice of source populations for restoration, or in genetic engineering. OUTLOOK A more unified platform will better convey the value of evolutionary methods to the public, scientists, and decision-makers. For researchers and practitioners, applications may be expanded to other disciplines, such as in the transfer of refuge strategies that slow resistance evolution in agriculture to slow unwanted evolution elsewhere (for example, cancer resistance or harvest-induced evolution). For policy-makers, adoption of practices that minimize unwanted evolution and reduce phenotype-environment mismatch in valued species is likely essential to achieve the forthcoming Sustainable Development Goals and the 2020 Aichi Biodiversity Targets. Exploiting evolution for humanitys sake Using artificial selection, humans have tapped into evolutionary processes for thousands of years. The results of this process we see all around us, from the dogs we share our homes with to the food we put on our table. Carroll et al. review the ways that a more intentional harnessing of evolution may be able to help us meet some of Earths most pressing challenges, including disease, climate change, and food security. Science, this issue 10.1126/science.1245993 Two categories of evolutionary challenges result from escalating human impacts on the planet. The first arises from cancers, pathogens, and pests that evolve too quickly and the second, from the inability of many valued species to adapt quickly enough. Applied evolutionary biology provides a suite of strategies to address these global challenges that threaten human health, food security, and biodiversity. This Review highlights both progress and gaps in genetic, developmental, and environmental manipulations across the life sciences that either target the rate and direction of evolution or reduce the mismatch between organisms and human-altered environments. Increased development and application of these underused tools will be vital in meeting current and future targets for sustainable development.

Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug

With reciprocal rearing experiments, we tested the hypothesis that adaptive differences in host-use traits among soapberry bug populations have a genetic basis. These experiments were conducted with two host races from Florida, an ‘ancestral-type’ one on a native host plant species and a ‘derived’ one on a recently introduced plant species (colonized mainly post-1950), on whose seed crops this insect depends for growth and reproduction. Compared to the native host species, the introduced host produces larger seed crops over a much briefer annual period. Its seeds are also significantly higher in lipids and lower in nitrogen. The bug populations exhibit greater juvenile survivorship on their ‘home’ hosts; that is, the derived population survives better on seeds of the introduced host than does its ancestral-type counterpart, and vice versa. Regardless of the rearing host, populations from the introduced host lay much smaller eggs, and fecundity measures show a more complex pattern than does survivorship: the ancestral-type population produces eggs at the same rate on each host, while the derived population is less fecund on the native host and exhibits enhanced fecundity on the introduced host. These results indicate that the population differences are evolved rather than host-induced. They appear to be adaptive responses to host differences in the spatial and temporal distribution of seed availability and nutritional quality, and show that increased performance on the alien host has evolved with surprising speed and magnitude, with concomitant reductions in performance on the original host.

Conciliation biology: the eco-evolutionary management of permanently invaded biotic systems.

Biotic invaders and similar anthropogenic novelties such as domesticates, transgenics, and cancers can alter ecology and evolution in environmental, agricultural, natural resource, public health, and medical systems. The resulting biological changes may either hinder or serve management objectives. For example, biological control and eradication programs are often defeated by unanticipated resistance evolution and by irreversibility of invader impacts. Moreover, eradication may be ill‐advised when nonnatives introduce beneficial functions. Thus, contexts that appear to call for eradication may instead demand managed coexistence of natives with nonnatives, and yet applied biologists have not generally considered the need to manage the eco‐evolutionary dynamics that commonly result from interactions of natives with nonnatives. Here, I advocate a conciliatory approach to managing systems where novel organisms cannot or should not be eradicated. Conciliatory strategies incorporate benefits of nonnatives to address many practical needs including slowing rates of resistance evolution, promoting evolution of indigenous biological control, cultivating replacement services and novel functions, and managing native–nonnative coevolution. Evolutionary links across disciplines foster cohesion essential for managing the broad impacts of novel biotic systems. Rather than signaling defeat, conciliation biology thus utilizes the predictive power of evolutionary theory to offer diverse and flexible pathways to more sustainable outcomes.

PMD, a Registered Botanical Mosquito Repellent with Deet-Like Efficacy

ABSTRACT para-Menthane-3,8-diol(PMD) is a monoterpene spent product of the distillation of leaves of the Australian lemon-scented gum tree (updated nomenclature Corymbia citriodora ssp. citriodora). In April 2005, the U.S. Centers for Disease Control and Prevention (CDC) endorsed two non-deet mosquito repellents, including PMD. However, few mosquito professionals have in-depth familiarity with the history and efficacy of PMD. In this article, we describe the origin and development of PMD as a repellent and offer a comprehensive review of its performance against Aedes, Anopheles, Culex, and Ochlerotatus. In addition, we present original data from field and laboratory studies involving large numbers of subjects and comparisons with high-concentration deet and other repellents. We conclude that not only is the CDC endorsement warranted but also that it probably underestimates the value of PMD as a deet alternative for public health applications.

The biology of post-invasion events

In this contribution we consider the biology of invading organisms after they have become established. Adaptive radiation over the long term has been a favorite subject in evolutionary biology. Examples have been Darwins finches in the Galapagos and the honeycreepers and Droscphila of Hawaii. Hawaiian honeycreepers have evolved from a finch-like ancestor into guilds of seed eaters, nectar feeders, and combined nectar and insect feeders plus some species with unique beak structures. In the Hawaiian Drosophila sexual selection may have driven the extensive adaptive radiation and speciation in the group. The North American soapberry bug Jadera haemotoloma is an interesting model for post-invasion evolution in the short term. Some populations have moved onto introduced goldenrain trees Koelreuteria spp. and have evolved different stylet (mouthpart) lengths, as a function o f fruit size, and new host preferences, all within the last 50 years. These rapid responses are possible because of high additive genetic variances for these traits. Similarly, there has been rapid evolution of life history variation in American shad introduced from east coast to west coast rivers. We postulate that invaders most likely to integrate successfully are those in which high levels of additive genetic variation are expressed in traits most likely to be adaptive in the new environment. Copyright

Birds, bugs and blood: avian parasitism and conservation

Parasitism has far-reaching implications not only for the ecology and evolution of species but also for conservation. The effects of blood-feeding ectoparasites on colonially nesting bird species have been wodely studied, but recent surprising reports show that solitarily nesting species are also commonly attacked, mainly by the larvae of flies. Most bird species are solitary nesters; as their habitats are increasingly fragmented, how will the potential for such parasitism be affected? One example is that of the endangered Puerto Rican parrot (Amazona vittata), in which habitat changes have introduced a deadly parasitic fly species in a complex and unpredicted manner. As theories on habitat fragmentation outpace the data, we need to carry out more field studies of the interactions between fragmentation and parasitism, and to include parasitism in species survival and recovery plans.