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Eco‐evolutionary rescue promotes host–pathogen coexistence

Emerging infectious pathogens are responsible for some of the most severe host mass mortality events in wild populations. Yet, effective pathogen control strategies are notoriously difficult to identify, in part because quantifying and forecasting pathogen spread and disease dynamics is challenging. Following an outbreak, hosts must cope with the presence of the pathogen, leading to host–pathogen coexistence or extirpation. Despite decades of research, little is known about host–pathogen coexistence post‐outbreak when low host abundances and cryptic species make these interactions difficult to study. Using a novel disease‐structured N‐mixture model, we evaluate empirical support for three host–pathogen coexistence hypotheses (source–sink, eco‐evolutionary rescue, and spatial variation in pathogen transmission) in a Neotropical amphibian community decimated by Batrachochytrium dendrobatidis ( Bd ) in 2004. During 2010–2014, we surveyed amphibians in Parque Nacional G. D. Omar Torríjos Herrera, Coclé Province, El Copé, Panama. We found that the primary driver of host–pathogen coexistence was eco‐evolutionary rescue, as evidenced by similar amphibian survival and recruitment rates between infected and uninfected hosts. Average apparent monthly survival rates of uninfected and infected hosts were both close to 96%, and the expected number of uninfected and infected hosts recruited (via immigration/reproduction) was less than one host per disease state per 20‐m site. The secondary driver of host–pathogen coexistence was spatial variation in pathogen transmission as we found that transmission was highest in areas of low abundance but there was no support for the source–sink hypothesis. Our results indicate that changes in the host community (i.e., through genetic or species composition) can reduce the impacts of emerging infectious disease post‐outbreak. Our disease‐structured N‐mixture model represents a valuable advancement for conservation managers trying to understand underlying host–pathogen interactions and provides new opportunities to study disease dynamics in remnant host populations decimated by virulent pathogens.

Ecological Applications

Estimating rates of local extinction and colonization in colonial species and an extension to the metapopulation and community levels

Coloniality has mainly been studied from an evolutionary perspective, but relatively few studies have developed methods for modelling colony dynamics. Changes in number of colonies over time provide a useful tool for predicting and evaluating the responses of colonial species to management and to environmental disturbance. Probabilistic Markov process models have been recently used to estimate colony site dynamics using presence–absence data when all colonies are detected in sampling efforts. Here, we define and develop two general approaches for the modelling and analysis of colony dynamics for sampling situations in which all colonies are, and are not, detected. For both approaches, we develop a general probabilistic model for the data and then constrain model parameters based on various hypotheses about colony dynamics. We use Akaike's Information Criterion (AIC) to assess the adequacy of the constrained models. The models are parameterised with conditional probabilities of local colony site extinction and colonization. Presence–absence data arising from Pollock's robust capture–recapture design provide the basis for obtaining unbiased estimates of extinction, colonization, and detection probabilities when not all colonies are detected. This second approach should be particularly useful in situations where detection probabilities are heterogeneous among colony sites. The general methodology is illustrated using presence–absence data on two species of herons. Estimates of the extinction and colonization rates showed interspecific differences and strong temporal and spatial variations. We were also able to test specific predictions about colony dynamics based on ideas about habitat change and metapopulation dynamics. We recommend estimators based on probabilistic modelling for future work on colony dynamics. We also believe that this methodological framework has wide application to problems in animal ecology concerning metapopulation and community dynamics.

Oikos

Size selection from fishways and potential evolutionary responses in a threatened Atlantic salmon population

The evolutionary effects of harvest on wild fish populations have been documented around the world; however, sublethal selective pressures can also cause evolutionary changes in phenotypes. For migratory fishes, passage facilities may represent instances of nonlethal selective pressure. Our analysis of 6 years of passage data suggests that certain fish passage facilities on the Penobscot River have been exerting selective pressure against large-bodied, anadromous Atlantic salmon ( Salmo salar ). At the second and third dams in the river, a 91-cm salmon was 21%–27% and 12%–16% less likely to pass than a 45-cm salmon, respectively. Fish size positively influences egg survival and number and is a heritable trait. Therefore, in a wild-reproducing population, exclusion of large fish from spawning areas may have population-level impacts. In the Penobscot River, most returning adults derive from a hatchery program that collects its broodstock after passing the first dam in the river. Analysis of fork lengths of salmon returning to the Penobscot River from 1978 to 2012 provided mixed support for evolution of size at maturity in different age classes in a pattern that may be expected from interactions with conservation hatchery operations. Additionally, slow-maturing and iteroparous individuals that represent the largest salmon size classes were essentially lost from the population during that time, and Penobscot River fish have shorter fork lengths at maturity than Atlantic salmon in undammed systems.

Maine

Phylogenetic risk assessment is robust for forecasting the impact of European insects on North American conifers

Some introduced species cause severe damage, although the majority have little impact. Robust predictions of which species are most likely to cause substantial impacts could focus efforts to mitigate those impacts or prevent certain invasions entirely. Introduced herbivorous insects can reduce crop yield, fundamentally alter natural and managed forest ecosystems, and are unique among invasive species in that they require certain host plants to succeed. Recent studies have demonstrated that understanding the evolutionary history of introduced herbivores and their host plants can provide robust predictions of impact. Specifically, divergence times between hosts in the native and introduced ranges of a nonnative insect can be used to predict the potential impact of the insect should it establish in a novel ecosystem. However, divergence time estimates vary among published phylogenetic datasets, making it crucial to understand if and how the choice of phylogeny affects prediction of impact. Here, we tested the robustness of impact prediction to variation in host phylogeny by using insects that feed on conifers and predicting the likelihood of high impact using four different published phylogenies. Our analyses ranked 62 insects that are not established in North America and 47 North American conifer species according to overall risk and vulnerability, respectively. We found that results were robust to the choice of phylogeny. Although published vascular plant phylogenies continue to be refined, our analysis indicates that those differences are not substantial enough to alter the predictions of invader impact. Our results can assist in focusing biosecurity programs for conifer pests and can be more generally applied to nonnative insects and their potential hosts by prioritizing surveillance for those insects most likely to be damaging invaders.

Ecological Applications

The future of biocontrol in the Anthropocene: A review of climate change impacts on biocontrol agents and their hosts

Biological control, the practice of using one species (biocontrol agent) to control the population of another (a host or prey species, hereafter target), can be a successful method to reduce pest species in agricultural and natural systems worldwide. Successful biocontrol agents often share a deep evolutionary history with their targets that results in high target specificity and synchronized phenology. However, with rapidly changing climatic conditions, users of biocontrol agents have questioned how climate change will affect both well-established and more recent biological control relationships. Using a meta-analysis of data collected from a systematic literature review, we evaluated the evidence for the impact of changing temperatures on the efficacy of biocontrol agents and corresponding responses in their targets. Overall, most studies of climate change impacts on biocontrol agents take place in the laboratory and focus on arthropod agents that are parasitoids. Results from our meta-analysis reveal that changes in temperature are projected to impact biocontrol agents and their targets similarly, with no overall significant changes to biocontrol agent or target performance. However, our results also show that temperature responses vary widely across study systems, as illustrated by case studies showing both positive, neutral, and negative effects of temperature on biocontrol agent efficacy, as well as variation in responses across the three core biological control measures of success: survival, reproduction, and efficacy. Our work highlights important knowledge gaps including how climate change will affect both biocontrol agents and their targets simultaneously. Additionally, we find that most current studies of climate impacts examined temperature relationships, predominantly of agricultural biocontrol agents. Increasing the breadth of studies is crucial for understanding the potential for climate change to affect the success of current and future biological control programs.

Ecological Applications

Late-kinematic timing of orogenic gold deposits and significance for computer-based exploration techniques with emphasis on the Yilgarn Block, Western Australia

Orogenic gold deposits are a widespread coherent group of epigenetic ore deposits that are sited in accretionary or collisional orogens. They formed over a large crustal-depth range from deep-seated low-salinity H 2 O–CO 2 ±CH 4 ±N 2 ore fluids and with Au transported as thio-complexes. Regional structures provide the main control on deposit distribution. In many terranes, first-order faults or shear zones appear to have controlled regional fluid flow, with greatest ore-fluid fluxes in, and adjacent to, lower-order faults, shear zones and/or large folds. Highly competent and/or chemically reactive rocks are the most common hosts to the larger deposits. Focusing of supralithostatic ore fluids into dilatant zones appears to occur late during the evolutionary history of the host terranes, normally within D 3 or D 4 in a D 1 –D 4 deformation sequence. Reactivation of suitably oriented pre-existing structures during a change in far-field stress orientation is a factor common to many deposits, and repeated reactivation may account for multiple mineralization episodes in some larger deposits. Absolute robust ages of mineralization support their late-kinematic timing, and, in general, suggest that deposits formed diachronously towards the end of the 100 to 200 m.y. long evolutionary history of hosting orogens. For example, in the Yilgarn Block, a region specifically emphasised in this study, orogenic gold deposits formed in the time interval between 40 and 90 m.y., with most about 60 to 70 m.y., after the youngest widespread basic-ultrabasic volcanism and towards the end of felsic magmatism. The late timing of orogenic gold deposits is pivotal to geologically-based exploration methodologies. This is because the present structural geometries of: (i) the deposits, (ii) the hosting goldfields, and (iii) the enclosing terranes are all essentially similar to those during gold mineralization, at least in their relative position to each other. Thus, interpretation of geological maps and cross-sections and three-dimensional models can be used to accurately simulate the physical conditions that existed at the time of ore deposition. It is particularly significant that the deposits are commonly related to repetitive and predictable geometries, such as structural heterogeneities within or adjacent to first-order structures, around rigid granitoid bodies, or in specific “locked-up” fold-thrust structures. Importantly, the two giant greenstone-hosted goldfields, Kalgoorlie and Timmins, show a remarkably similar geometry at the regional scale. Computer-based stress mapping and GIS-based prospectivity mapping are two computer-based quantitative methodologies that can utilize and take advantage of the late timing aspect of this deposit type to provide important geological aids in exploration, both in broad regions and more localized goldfields. Both require an accurate and consistent solid geology map, stress mapping requires knowledge of the far-field stresses during mineralization, and the empirical prospectivity mapping requires data from a significant number of known deposits in the terrane. The Kalgoorlie Terrane, in the Yilgarn Block, meets these criteria, and illustrates the potential of these methodologies in the exploration for orogenic gold deposits. Low minimum stress anomalies, interpreted to represent dilational zones during gold-related deformation, coincide well with the positions of known goldfields rather than individual gold deposits in the terrane, and there are additional as-yet unexplained anomalies. The prospectivity analysis confirms that predictable and repetitive factors controlling the siting of deposits are: (i) proximity to, and orientation and curvature of, granitoid-greenstone contacts, (ii) proximity to segments of crustal faults which strike in a preferred direction, (iii) proximity to specific lithological contacts which have similar preferred strike, (iv) proximity to anticlinal structures, and (v) the presence of preferred reactive host rocks (e.g., dolerite). The prospectivity map defines a series of anomalous areas, which broadly conform to those of the stress map (>78% correspondence). The most prospective category on this map covers less than 0.3% of the greenstone belts and yet hosts 16% of the known deposits, which have produced>80% of known gold. Thus, it discriminates in favour of the larger economically more-attractive deposits in the terrane. The successful application of stress mapping and prospectivity mapping to geology-based exploration for orogenic gold deposits indicates that more quantitative analysis of geological map data is a profitable line of research. The computer-based nature of these methodologies is ideal for the production of an ultimate, integrated, deposit target map, which can be compared to other, more conventional, targeting parameters such as geophysical and geochemical anomalies. Such an integrated strategy appears the way forward in the increasingly difficult task of cost-effective global exploration for orogenic gold deposits in poorly exposed terranes.

Western Australia

Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.

Ecological Applications