A framework to integrate innovations in invasion science for proactive management.

Invasive alien species (IAS) are a rising threat to biodiversity, national security, and regional economies, with impacts in the hundreds of billions of U.S. dollars annually. Proactive or predictive approaches guided by scientific knowledge are essential to keeping pace with growing impacts of invasions under climate change. Although the rapid development of diverse technologies and approaches has produced tools with the potential to greatly accelerate invasion research and management, innovation has far outpaced implementation and coordination. Technological and methodological syntheses are urgently needed to close the growing implementation gap and facilitate interdisciplinary collaboration and synergy among evolving disciplines. A broad review is necessary to demonstrate the utility and relevance of work in diverse fields to generate actionable science for the ongoing invasion crisis. Here, we review such advances in relevant fields including remote sensing, epidemiology, big data analytics, environmental DNA (eDNA) sampling, genomics, and others, and present a generalized framework for distilling existing and emerging data into products for proactive IAS research and management. This integrated workflow provides a pathway for scientists and practitioners in diverse disciplines to contribute to applied invasion biology in a coordinated, synergistic, and scalable manner.

Strategic considerations for invasive species managers in the utilization of environmental DNA (eDNA): steps for incorporating this powerful surveillance tool.

Invasive species surveillance programs can utilize environmental DNA sampling and analysis to provide information on the presence of invasive species. Wider utilization of eDNA techniques for invasive species surveillance may be warranted. This paper covers topics directed towards invasive species managers and eDNA practitioners working at the intersection of eDNA techniques and invasive species surveillance. It provides background information on the utility of eDNA for invasive species management and points to various examples of its use across federal and international programs. It provides information on 1) why an invasive species manager should consider using eDNA, 2) deciding if eDNA can help with the manager's surveillance needs, 3) important components to operational implementation, and 4) a high-level overview of the technical steps necessary for eDNA analysis. The goal of this paper is to assist invasive species managers in deciding if, when, and how to use eDNA for surveillance. If eDNA use is elected, the paper provides guidance on steps to ensure a clear understanding of the strengths and limitation of the methods and how results can be best utilized in the context of invasive species surveillance.

Towards connecting biodiversity and geodiversity across scales with satellite remote sensing.

ISSUE: Geodiversity (i.e., the variation in Earth's abiotic processes and features) has strong effects on biodiversity patterns. However, major gaps remain in our understanding of how relationships between biodiversity and geodiversity vary over space and time. Biodiversity data are globally sparse and concentrated in particular regions. In contrast, many forms of geodiversity can be measured continuously across the globe with satellite remote sensing. Satellite remote sensing directly measures environmental variables with grain sizes as small as tens of metres and can therefore elucidate biodiversity-geodiversity relationships across scales. EVIDENCE: We show how one important geodiversity variable, elevation, relates to alpha, beta and gamma taxonomic diversity of trees across spatial scales. We use elevation from NASA's Shuttle Radar Topography Mission (SRTM) and c. 16,000 Forest Inventory and Analysis plots to quantify spatial scaling relationships between biodiversity and geodiversity with generalized linear models (for alpha and gamma diversity) and beta regression (for beta diversity) across five spatial grains ranging from 5 to 100 km. We illustrate different relationships depending on the form of diversity; beta and gamma diversity show the strongest relationship with variation in elevation. CONCLUSION: With the onset of climate change, it is more important than ever to examine geodiversity for its potential to foster biodiversity. Widely available satellite remotely sensed geodiversity data offer an important and expanding suite of measurements for understanding and predicting changes in different forms of biodiversity across scales. Interdisciplinary research teams spanning biodiversity, geoscience and remote sensing are well poised to advance understanding of biodiversity-geodiversity relationships across scales and guide the conservation of nature.

Landscape genomic insights into the historic migration of mountain hemlock in response to Holocene climate change.

PREMISE OF THE STUDY: Untangling alternative historic dispersal pathways in long-lived tree species is critical to better understand how temperate tree species may respond to climatic change. However, disentangling these alternative pathways is often difficult. Emerging genomic technologies and landscape genetics techniques improve our ability to assess these pathways in natural systems. We address the question to what degree have microrefugial patches and long-distance dispersal been responsible for the colonization of mountain hemlock (Tsuga mertensiana) on the Alaskan Kenai Peninsula. METHODS: We used double-digest restriction-associated DNA sequencing (ddRADseq) to identify genetic variants across eight mountain hemlock sample sites on the Kenai Peninsula, Alaska. We assessed genetic diversity and linkage disequilibrium using landscape and population genetics approaches. Alternative historic dispersal pathways were assessed using discriminant analysis of principle components and electrical circuit theory. KEY RESULTS: A combination of decreasing diversity, high gene flow, and landscape connectivity indicates that mountain hemlock colonization on the Kenai Peninsula is the result of long-distance dispersal. We found that contemporary climate best explained gene flow patterns and that isolation by resistance was a better model explaining genetic variation than isolation by distance. CONCLUSIONS: Our findings support the conclusion that mountain hemlock colonization is the result of several long-distance dispersal events following Pleistocene glaciation. The high dispersal capability suggests that mountain hemlock may be able to respond to future climate change and expand its range as new habitat opens along its northern distribution.

Reading between the vines: Hosts as islands for extreme holoparasitic plants.

PREMISE OF THE STUDY: Partitioning of population genetic variation in plants may be affected by numerous factors including life history and dispersal characteristics. In parasitic plants, interactions with host populations may be an additional factor influencing partitioning. To test for hierarchical population genetic patterns related to obligate endoparasitism, we studied three species of Rafflesiaceae, which grow as extremely reduced endophytes infecting Tetrastigma vines in Southeast Asia. METHODS: Microsatellite markers were developed and multilocus genotypes were determined for Rafflesia cantleyi, Rafflesia tuan-mudae, and Sapria himalayana and each of their Tetrastigma hosts. Relatedness among parasite individuals was estimated, and AMOVAs were used to determine levels of population genetic subdivision. KEY RESULTS: Microsatellite genotypes for 340 paired parasite and host samples revealed that host vines were infected by numerous Rafflesiaceae individuals that may spread for up to 14 m within stem tissues. Surprisingly, Rafflesiaceae parasites within a given host are significantly more closely related to each other than individuals of the same species in other host individuals. The pattern of hierarchical population genetic subdivision we detected across species is likely due to limited seed dispersal with reinfection of natal host vines. CONCLUSIONS: These findings demonstrate common population genetic patterns between animal and plant parasites, potentially indicating advantages of close relatives infecting hosts. This study also has important conservation implications for Rafflesiaceae since our data suggest that destruction of a single infected host vine could result in large genetic losses.

Association of genetic and phenotypic variability with geography and climate in three southern California oaks.

PREMISE OF THE STUDY: Geography and climate shape the distribution of organisms, their genotypes, and their phenotypes. To understand historical and future evolutionary and ecological responses to climate, we compared the association of geography and climate of three oak species (Quercus engelmannii, Quercus berberidifolia, and Quercus cornelius-mulleri) in an environmentally heterogeneous region of southern California at three organizational levels: regional species distributions, genetic variation, and phenotypic variation. METHODS: We identified climatic variables influencing regional distribution patterns using species distribution models (SDMs), and then tested whether those individual variables are important in shaping genetic (microsatellite) and phenotypic (leaf morphology) variation. We estimated the relative contributions of geography and climate using multivariate redundancy analyses (RDA) with variance partitioning. KEY RESULTS: The modeled distribution of each species was influenced by climate differently. Our analysis of genetic variation using RDA identified small but significant associations between genetic variation with climate and geography in Q. engelmannii and Q. cornelius-mulleri, but not in Q. berberidifolia, and climate explained more of the variation. Our analysis of phenotypic variation in Q. engelmannii indicated that climate had more impact than geography, but not in Q. berberidifolia. Throughout our analyses, we did not find a consistent pattern in effects of individual climatic variables. CONCLUSIONS: Our comparative analysis illustrates that climate influences tree response at all organizational levels, but the important climate factors vary depending on the level and on the species. Because of these species-specific and level-specific responses, today's sympatric species are unlikely to have similar distributions in the future.

Effect of clonal reproduction on genetic structure in Pentaclethra macroloba (Fabaceae: Mimosoideae).

The existence of monodominant forests on well-drained soils in tropical regions has been widely reported. Such forests most likely result from a combination of both ecological and evolutionary factors. Under conditions of high seed and seedling mortality, vegetative reproduction could create a reproductive advantage leading to forest dominance, and profoundly affect the distribution of genetic variation in a clonal species. We investigated these effects in a low diversity forest site in Northeastern Costa Rica dominated by the species Pentaclethra macroloba, which sprouts from the root mass of fallen trees and from snapped trunks. We examined the population structure of juvenile P. macroloba growing in different soil types and across an elevational gradient. Using seven molecular markers, we genotyped 173 juvenile P. macroloba from 18 plots (six plots in seasonally inundated swamps, and 12 plots in upland non-swamp) spanning 50-300m in elevation at La Selva Biological Station and the adjacent Reserva Ecológica Bijagual in Northeastern Costa Rica. We answered two specific questions: (1) How extensive is clonal reproduction? and (2) what is the distribution of genetic diversity and structure? We found that clonal reproduction occurred exclusively within inundated swamp areas. However, there was no significant difference between genetic diversity measures in swamp and non-swamp plots, which were both generally low when compared with other tropical forest species. Genetic structure was significant across all plots (F(ST) = -0.109). However, genetic structure among swamp plots (F(ST) = 0.128) was higher than among non-swamp upland plots (F(ST) = 0.093). Additionally, spatial autocorrelation among individuals within non-swamp upland plots was significant from the 25 to 100m spatial scale, but not within swamp plots. The degree of overall genetic structure we found in P. macroloba is high for a tropical forest tree. The incidence of clonal reproduction is a contributing factor in genetic differentiation, but the high structure among plots without clonal reproduction indicates that other factors contribute as well.

Effect of clonal reproduction on genetic structure in Pentaclethra macroloba (Fabaceae: Mimosoideae) / Efecto de la reproducción clonal en la estructura genética de Pentaclethra macroloba (Fabaceae: Mimosoideae)

The existence of monodominant forests on well-drained soils in tropical regions has been widely reported. Such forests most likely result from a combination of both ecological and evolutionary factors. Under conditions of high seed and seedling mortality, vegetative reproduction could create a reproductive advantage leading to forest dominance, and profoundly affect the distribution of genetic variation in a clonal species. We investigated these effects in a low diversity forest site in Northeastern Costa Rica dominated by the species Pentaclethra macroloba, which sprouts from the root mass of fallen trees and from snapped trunks. We examined the population structure of juvenile P. macroloba growing in different soil types and across an elevational gradient. Using seven molecular markers, we genotyped 173 juvenile P. macroloba from 18 plots (six plots in seasonally inundated swamps, and 12 plots in upland non-swamp) spanning 50-300m in elevation at La Selva Biological Station and the adjacent Reserva Ecológica Bijagual in Northeastern Costa Rica. We answered two specific questions: (1) How extensive is clonal reproduction? and (2) what is the distribution of genetic diversity and structure?. We found that clonal reproduction occurred exclusively within inundated swamp areas. However, there was no significant difference between genetic diversity measures in swamp and non-swamp plots, which were both generally low when compared with other tropical forest species. Genetic structure was significant across all plots (F ST=0.109). However, genetic structure among swamp plots (F ST=0.128) was higher than among non-swamp upland plots (F ST=0.093). Additionally, spatial autocorrelation among individuals within non-swamp upland plots was significant from the 25 to 100m spatial scale, but not within swamp plots. The degree of overall genetic structure we found in P. macroloba is high for a tropical forest tree. The incidence of clonal reproduction is a contributing factor in genetic differentiation, but the high structure among plots without clonal reproduction indicates that other factors contribute as well.

La existencia de bosques monodominantes sobre suelos bien drenados en regiones tropicales ha sido ampliamente reportada. Investigaciones recientes han sugerido que tales bosques son probablemente resultado de una combinación de factores ecológicos y evolutivos. Bajo condiciones de alta mortalidad de semillas y plántulas, la reproducción vegetativa podría crear una ventaja reproductiva llevando a la dominancia del bosque, pero también podría afectar profundamente la distribución de la variación genética en especies clonales. Investigamos estos efectos en un sitio de bosque con baja diversidad de especies en el Noreste de Costa Rica que es ampliamente dominado por la especie Pentaclethra macroloba, la cual retoña de la masa de raíces de árboles caídos y de troncos partidos. Examinamos la estructura poblacional de individuos juveniles de P. macroloba creciendo en diferentes tipos de suelo y a través de un gradiente de altitud. Utilizamos siete marcadores moleculares, genotipamos 173 Pentaclethra macroloba de 18 parcelas (seis en ciénagas y 12 en ambientes no cenagosos) ubicados en un gradiente de elevación entre 50-300m en las reservas adyacentes: Reserva Biológica Bijagual y Estación Biológica La Selva, en el centro de Costa Rica. Abordamos dos preguntas específicas: (1) ¿Qué tan extensa es la reproducción clonal? y (2) ¿Cuál es la distribución de diversidad y estructura genética? Encontramos que la reproducción clonal ocurrió exclusivamente dentro de áreas cenagosas inundadas. La estructura genética fue significativa en todas las parcelas (F ST=0.109). Observamos una estructura genética más alta entre poblaciones juveniles dentro de las ciénagas (F ST=0.128) comparada con poblaciones no cenagosas en parcelas a mayor altura (F ST=0.093), con mayor autocorrelación espacial en sitios no cenagosos en el intervalo entre 25 y 100m. La presencia de reproducción clonal no afectó significativamente las medidas de diversidad entre las dos áreas, que fueron generalmente bajas comparadas con otras especies de bosque tropical. El alto grado de estructura genética en general es novedoso para un árbol de bosque tropical. La incidencia de reproducción clonal es un factor que contribuye en la diferenciación genética, pero la alta estructura en parcelas sin reproducción clonal indica que otros factores están contribuyendo también.