An integrative phenology and climatic suitability model for emerald ash borer.

Introduction: Decision support models that predict both when and where to expect emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), are needed for the development and implementation of effective management strategies against this major invasive pest of ash (Fraxinus species) in North America and other regions such as Europe. We present a spatialized model of phenology and climatic suitability for EAB for use in the Degree-Days, Risk, and Phenological event mapping (DDRP) platform, which is an open-source decision support tool to help detect, monitor, and manage invasive threats. Methods: We evaluated the model using presence records from three geographic regions (China, North America, and Europe) and a phenological dataset consisting primarily of observations from the northeastern and midwestern United States. To demonstrate the model, we produced phenological event maps for a recent year and tested for trends in EAB's phenology and potential distribution over a recent 20-year period. Results: Overall, the model exhibited strong performance. Presence was correctly estimated for over 99% of presence records and predicted dates of adult phenological events corresponded closely with observed dates, with a mean absolute error of ca. 7 days and low estimates of bias. Climate stresses were insufficient to exclude EAB from areas with native Fraxinus species in North America and Europe; however, extreme weather events, climate warming, and an inability for EAB to complete its life cycle may reduce suitability for some areas. Significant trends toward earlier adult emergence over 20 years occurred in only some areas. Discussion: Near real-time model forecasts for the conterminous United States are available at two websites to provide end-users with decision-support for surveillance and management of this invasive pest. Forecasts of adult emergence and egg hatch are particularly relevant for surveillance and for managing existing populations with pesticide treatments and parasitoid introductions.

Phenological Mapping of Invasive Insects: Decision Support for Surveillance and Management.

Readily accessible and easily understood forecasts of the phenology of invasive insects have the potential to support and improve strategic and tactical decisions for insect surveillance and management. However, most phenological modeling tools developed to date are site-based, meaning that they use data from a weather station to produce forecasts for that single site. Spatial forecasts of phenology, or phenological maps, are more useful for decision-making at area-wide scales, such as counties, states, or entire nations. In this review, we provide a brief history on the development of phenological mapping technologies with a focus on degree-day models and their use as decision support tools for invasive insect species. We compare three different types of phenological maps and provide examples using outputs of web-based platforms that are presently available for real-time mapping of invasive insects for the contiguous United States. Next, we summarize sources of climate data available for real-time mapping, applications of phenological maps, strategies for balancing model complexity and simplicity, data sources and methods for validating spatial phenology models, and potential sources of model error and uncertainty. Lastly, we make suggestions for future research that may improve the quality and utility of phenological maps for invasive insects.

Potential Distribution of Invasive Boxwood Blight Pathogen (Calonectriapseudonaviculata) as Predicted by Process-Based and Correlative Models.

Boxwood blight caused by Cps is an emerging disease that has had devastating impacts on Buxus spp. in the horticultural sector, landscapes, and native ecosystems. In this study, we produced a process-based climatic suitability model in the CLIMEX program and combined outputs of four different correlative modeling algorithms to generate an ensemble correlative model. All models were fit and validated using a presence record dataset comprised of Cps detections across its entire known invaded range. Evaluations of model performance provided validation of good model fit for all models. A consensus map of CLIMEX and ensemble correlative model predictions indicated that not-yet-invaded areas in eastern and southern Europe and in the southeastern, midwestern, and Pacific coast regions of North America are climatically suitable for Cps establishment. Most regions of the world where Buxus and its congeners are native are also at risk of establishment. These findings provide the first insights into Cps global invasion threat, suggesting that this invasive pathogen has the potential to significantly expand its range.

DDRP: Real-time phenology and climatic suitability modeling of invasive insects.

Rapidly detecting and responding to new invasive species and the spread of those that are already established is essential for reducing their potential threat to food production, the economy, and the environment. We describe a new spatial modeling platform that integrates mapping of phenology and climatic suitability in real-time to provide timely and comprehensive guidance for stakeholders needing to know both where and when invasive insect species could potentially invade the conterminous United States. The Degree-Days, Risk, and Phenological event mapping (DDRP) platform serves as an open-source and relatively easy-to-parameterize decision support tool to help detect new invasive threats, schedule monitoring and management actions, optimize biological control, and predict potential impacts on agricultural production. DDRP uses a process-based modeling approach in which degree-days and temperature stress are calculated daily and accumulate over time to model phenology and climatic suitability, respectively. Outputs include predictions of the number of completed generations, life stages present, dates of phenological events, and climatically suitable areas based on two levels of climate stress. Species parameter values can be derived from laboratory and field studies or estimated through an additional modeling step. DDRP is written entirely in R, making it flexible and extensible, and capitalizes on multiple R packages to generate gridded and graphical outputs. We illustrate the DDRP modeling platform and the process of model parameterization using two invasive insect species as example threats to United States agriculture: the light brown apple moth, Epiphyas postvittana, and the small tomato borer, Neoleucinodes elegantalis. We then discuss example applications of DDRP as a decision support tool, review its potential limitations and sources of model error, and outline some ideas for future improvements to the platform.

Expansion history and environmental suitability shape effective population size in a plant invasion.

The margins of an expanding range are predicted to be challenging environments for adaptation. Marginal populations should often experience low effective population sizes (Ne ) where genetic drift is high due to demographic expansion and/or census population size is low due to unfavourable environmental conditions. Nevertheless, invasive species demonstrate increasing evidence of rapid evolution and potential adaptation to novel environments encountered during colonization, calling into question whether significant reductions in Ne are realized during range expansions in nature. Here we report one of the first empirical tests of the joint effects of expansion dynamics and environment on effective population size variation during invasive range expansion. We estimate contemporary values of Ne using rates of linkage disequilibrium among genome-wide markers within introduced populations of the highly invasive plant Centaurea solstitialis (yellow starthistle) in North America (California, USA), and within native Eurasian populations. As predicted, we find that Ne within the invaded range is positively correlated with both expansion history (time since founding) and habitat quality (abiotic climate). History and climate had independent additive effects with similar effect sizes, indicating an important role for both factors in this invasion. These results support theoretical expectations for the population genetics of range expansion, though whether these processes can ultimately arrest the spread of an invasive species remains an unanswered question.

Potential limits to the benefits of admixture during biological invasion.

Species introductions often bring together genetically divergent source populations, resulting in genetic admixture. This geographic reshuffling of diversity has the potential to generate favourable new genetic combinations, facilitating the establishment and invasive spread of introduced populations. Observational support for the superior performance of admixed introductions has been mixed, however, and the broad importance of admixture to invasion questioned. Under most underlying mechanisms, admixture's benefits should be expected to increase with greater divergence among and lower genetic diversity within source populations, though these effects have not been quantified in invaders. We experimentally crossed source populations differing in divergence in the invasive plant Centaurea solstitialis. Crosses resulted in many positive (heterotic) interactions, but fitness benefits declined and were ultimately negative at high source divergence, with patterns suggesting cytonuclear epistasis. We explored the literature to assess whether such negative epistatic interactions might be impeding admixture at high source population divergence. Admixed introductions reported for plants came from sources with a wide range of genetic variation, but were disproportionately absent where there was high genetic divergence among native populations. We conclude that while admixture is common in species introductions and often happens under conditions expected to be beneficial to invaders, these conditions may be constrained by predictable negative genetic interactions, potentially explaining conflicting evidence for admixture's benefits to invasion.

ORIGINS AND GENETIC DIVERSITY OF INTRODUCED POPULATIONS OF THE PUERTO RICAN RED-EYED COQUÍ, ELEUTHERODACTYLUS ANTILLENSIS, IN SAINT CROIX (U.S. VIRGIN ISLANDS) AND PANAMÁ.

The Red-eyed Coquí, Eleutherodactylus antillensis, is a terrestrial frog endemic to the Puerto Rican Bank (Puerto Rico and numerous islands and cays off its eastern coast), in the eastern Caribbean Sea. The species was likely introduced in Saint Croix, an island c. 100 km southeast of Puerto Rico, in the late 1930s, and in Panamá City, Panamá, in the late 1950s or early 1960s, but the source(s) of these introductions are unknown. We analyzed sequence data from one mtDNA locus and four nuDNA introns to infer the origin(s) of the Saint Croix and Panamá City populations and quantify their genetic diversity. Saint Croix and Panamanian populations do not share any haplotypes, and they cluster with different native populations, suggesting that they are derived from separate sources in the Puerto Rican Bank. Patterns of population structure trace the probable sources of E. antillensis in Saint Croix to islands off Puerto Rico's eastern coast, which include Vieques, Culebra, Saint Thomas, Saint John, Tortola, and Virgin Gorda, and possibly to eastern Puerto Rico as well. In contrast, Panamá City E. antillensis probably originated from either western or eastern Puerto Rico. Genetic diversity in the introduced populations is similar to or lower than in populations in the species' native range, indicating that genetic diversity has not increased in the alien frogs. Our findings may facilitate the development of preventive measures to minimize introductions of non-native amphibians in the Caribbean and Central America.

Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis).

Identifying sources of genetic variation and reconstructing invasion routes for non-native introduced species is central to understanding the circumstances under which they may evolve increased invasiveness. In this study, we used genome-wide single nucleotide polymorphisms to study the colonization history of Centaurea solstitialis in its native range in Eurasia and invasions into the Americas. We leveraged this information to pinpoint key evolutionary shifts in plant size, a focal trait associated with invasiveness in this species. Our analyses revealed clear population genomic structure of potential source populations in Eurasia, including deep differentiation of a lineage found in the southern Apennine and Balkan Peninsulas and divergence among populations in Asia, eastern Europe and western Europe. We found strongest support for an evolutionary scenario in which western European populations were derived from an ancient admixture event between populations from eastern Europe and Asia, and subsequently served as the main genetic 'bridgehead' for introductions to the Americas. Introductions to California appear to be from a single source region, and multiple, independent introductions of divergent genotypes likely occurred into the Pacific Northwest. Plant size has evolved significantly at three points during range expansion, including a large size increase in the lineage responsible for the aggressive invasion of the California interior. These results reveal a long history of colonization, admixture and trait evolution in C. solstitialis, and suggest routes for improving evidence-based management decisions for one of the most ecologically and economically damaging invasive species in the western United States.

Climate as a driver of tropical insular diversity: comparative phylogeography of two ecologically distinctive frogs in Puerto Rico.

The effects of late Quaternary climate on distributions and evolutionary dynamics of insular species are poorly understood in most tropical archipelagoes. We used ecological niche models under past and current climate to derive hypotheses regarding how stable climatic conditions shaped genetic diversity in two ecologically distinctive frogs in Puerto Rico. Whereas the Mountain Coquí, Eleutherodactylus portoricensis, is restricted to montane forest in the Cayey and Luquillo Mountains, the Red-eyed Coquí, E. antillensis, is a habitat generalist distributed across the entire Puerto Rican Bank (Puerto Rico and the Virgin Islands, excluding St. Croix). To test our hypotheses, we conducted phylogeographic and population genetic analyses based on mitochondrial and nuclear loci of each species across their range in Puerto Rico. Patterns of population differentiation in E. portoricensis, but not in E. antillensis, supported our hypotheses. For E. portoricensis, these patterns include: individuals isolated by long-term unsuitable climate in the Río Grande de Loíza Basin in eastern Puerto Rico belong to different genetic clusters; past and current climate strongly predicted genetic differentiation; and Cayey and Luquillo Mountains populations split prior to the last interglacial. For E. antillensis, these patterns include: genetic clusters did not fully correspond to predicted long-term unsuitable climate; and past and current climate weakly predicted patterns of genetic differentiation. Genetic signatures in E. antillensis are consistent with a recent range expansion into western Puerto Rico, possibly resulting from climate change and anthropogenic influences. As predicted, regions with a large area of long-term suitable climate were associated with higher genetic diversity in both species, suggesting larger and more stable populations. Finally, we discussed the implications of our findings for developing evidence-based management decisions for E. portoricensis, a taxon of special concern. Our findings illustrate the role of persistent suitable climatic conditions in promoting the persistence and diversification of tropical island organisms.

Evolution of invasiveness through increased resource use in a vacant niche.

Non-native plants are now a pervasive feature of ecosystems across the globe1. One hypothesis for this pattern is that introduced species occupy open niches in recipient communities2,3. If true, then non-native plants should often benefit from low competition for limiting resources that define niches. Many plants have evolved larger size after introduction, consistent with increased access to limiting resources4-9. It has been difficult to test whether larger size reflects adaptation to exploit open resources, however, because vacant niches are generally challenging to identify in plants. Here we take advantage of a situation in which a highly invasive non-native plant, Centaurea solstitialis L. (yellow starthistle, hereafter 'YST'), occupies a well-described environmental niche, wherein water is a known limiting resource10,11. We use a glasshouse common environment and climatic niche modeling to reveal that invading YST has evolved a higher-fitness life history at the expense of increased dependence on water. Critically, historical declines in resident competitors have made water more available for introduced plants11,12, demonstrating how native biodiversity declines can open niches and create opportunities for introduced species to evolve increased resource use, a potentially widespread basis for introduction success and the evolution of invasive life histories.

Population Declines of Mountain Coqui (Eleutherodactylus portoricensis) in the Cordillera Central of Puerto Rico.

The Mountain Coqui (Eleutherodactylus portoricensis) is a frog endemic to montane rainforests in the Cordillera Central and Luquillo Mountains of Puerto Rico. Classified as endangered by the IUCN Red List and as vulnerable by the Department of Natural and Environmental Resources of Puerto Rico, this species has undergone considerable decline in the Luquillo Mountains. To evaluate the population status of E. portoricensis across its entire range, we conducted ~87 hours of surveys at 18 historical localities and 25 additional localities that we considered suitable for this species. We generated occupancy models to estimate the probability of occurrence at surveyed sites and to identify geographic and climatic factors affecting site occupancy. We also constructed a suitability map to visualize population status in relation to the presence of land cover at elevations where the species has been documented, and determined the dates when populations were last detected at historical localities. Eleutherodactylus portoricensis was detected at 14 of 43 localities, including 10 of 18 historical localities, but it was not detected at any localities west of Aibonito (western Cordillera Central). Occupancy models estimated the probability of occurrence for localities in the western Cordillera Central as zero. Site occupancy was positively associated with montane cloud forest, and negatively associated with the western Cordillera Central, maximum temperature, and precipitation seasonality. The suitability map suggests that declines have occurred despite the presence of suitable habitat. We suggest upgrading the extinction risk of E. portoricensis and potentially developing a captive breeding program for this species.

Sea level, topography and island diversity: phylogeography of the Puerto Rican Red-eyed Coquí, Eleutherodactylus antillensis.

Quaternary climatic oscillations caused changes in sea level that altered the size, number and degree of isolation of islands, particularly in land-bridge archipelagoes. Elucidating the demographic effects of these oscillations increases our understanding of the role of climate change in shaping evolutionary processes in archipelagoes. The Puerto Rican Bank (PRB) (Puerto Rico and the Eastern Islands, which comprise Vieques, Culebra, the Virgin Islands and associated islets) in the eastern Caribbean Sea periodically coalesced during glaciations and fragmented during interglacial periods of the quaternary. To explore population-level consequences of sea level changes, we studied the phylogeography of the frog Eleutherodactylus antillensis across the archipelago. We tested hypotheses encompassing vicariance and dispersal narratives by sequencing mtDNA (c. 552 bp) of 285 individuals from 58 localities, and four nuDNA introns (totalling c. 1633 bp) from 173 of these individuals. We found low support for a hypothesis of divergence of the Eastern Islands populations prior to the start of the penultimate interglacial c. 250 kya, and higher support for a hypothesis of colonization of the Eastern Islands from sources in eastern Puerto Rico during the penultimate and last glacial period, when a land bridge united the PRB. The Río Grande de Loíza Basin in eastern Puerto Rico delineates a phylogeographic break. Haplotypes shared between the PRB and St. Croix (an island c. 105 km south-east of this archipelago) likely represent human-mediated introductions. Our findings illustrate how varying degrees of connectivity and isolation influence the evolution of tropical island organisms.

A test of the conjecture that G-matrices are more stable than B-matrices.

The G-matrix occupies an important position in evolutionary biology both as a summary of the inheritance of quantitative traits and as an ingredient in predicting how those traits will respond to selection and drift. Consequently, the stability of G has an important bearing on the accuracy of predicted evolutionary trajectories. Furthermore, G should evolve in response to stable features of the adaptive landscape and their trajectories through time. Although the stability and evolution of G might be predicted from knowledge of selection in natural populations, most empirical comparisons of G-matrices have been made in the absence of such a priori predictions. We present a theoretical argument that within-sex G-matrices should be more stable than between-sex B-matrices because they are more powerfully exposed to multivariate stabilizing selection. We tested this conjecture by comparing estimates of B- and within-sex G-matrices among three populations of the garter snake Thamnophis elegans. Matrix comparisons using Flury's hierarchical approach revealed that within-sex G-matrices had four principal components in common (full CPC), whereas B-matrices had only a single principal component in common and eigenvalues that were more variable among populations. These results suggest that within-sex G is more stable than B, as predicted by our theoretical argument.