Evolutionary epidemiology predicts the emergence of glyphosate resistance in a major agricultural weed

The evolution of resistance to herbicides is a striking example of rapid, human-directed adaptation with major consequences for food production. Most studies of herbicide resistance are performed reactively and focus on post-hoc determination of resistance mechanisms following the evolution of field resistance. If the evolution of resistance can be anticipated however, pro-active management to slow or prevent resistance traits evolving can be advocated. We report a national-scale study that combines population monitoring, glyphosate sensitivity assays, quantitative genetics and epidemiological analyses to pro-actively identify the prerequisites for adaptive evolution (directional selection and heritable genetic variation) to the world’s most widely used herbicide (glyphosate) in a major, economically damaging weed species, Alopecurus myosuroides. Results highlighted pronounced, heritable variability in glyphosate sensitivity amongst UK A. myosuroides populations. We demonstrated a direct epidemiological link between historical glyphosate selection and current population-level sensitivity, and show that current field populations respond to further glyphosate selection. This study provides a novel, pro-active assessment of adaptive potential for herbicide resistance, and provides compelling evidence of directional selection for glyphosate insensitivity in advance of reports of field resistance. The epidemiological approach developed can provide a basis for further pro-active study of resistance evolution across pesticide resistance disciplines

Dissecting weed adaptation: fitness and trait correlations in herbicide resistant Alopecurus myosuroides

BACKGROUND Unravelling the genetic architecture of non-target-site resistance (NTSR) traits in weed populations can inform questions about the inheritance, trade-offs and fitness costs associated with these traits. Classical quantitative genetics approaches allow study of the genetic architecture of polygenic traits even where the genetic basis of adaptation remains unknown. These approaches have the potential to overcome some of the limitations of previous studies into the genetics and fitness of NTSR. RESULTS Using a quantitative genetic analysis of 400 pedigreed Alopecurus myosuroides seed families from nine field-collected populations, we found strong heritability for resistance to the acetolactate synthase and acetyl CoA carboxylase inhibitors (h2 = 0.731 and 0.938, respectively), and evidence for shared additive genetic variance for resistance to these two different herbicide modes of action, rg = 0.34 (survival), 0.38 (biomass). We find no evidence for genetic correlations between life-history traits and herbicide resistance, indicating that resistance to these two modes of action is not associated with large fitness costs in blackgrass. We do, however, demonstrate that phenotypic variation in plant flowering characteristics is heritable, h2 = 0.213 (flower height), 0.529 (flower head number), 0.449 (time to flowering) and 0.372 (time to seed shed), demonstrating the potential for adaptation to other nonchemical management practices (e.g. mowing of flowering heads) now being adopted for blackgrass control. CONCLUSION These results highlight that quantitative genetics can provide important insight into the inheritance and genetic architecture of NTSR, and can be used alongside emerging molecular techniques to better understand the evolutionary and fitness landscape of herbicide resistance

Evolution of generalist resistance to herbicide mixtures reveals a trade-off in resistance management

Intense selection by pesticides and antibiotics has resulted in a global epidemic of evolved resistance. In agriculture and medicine, using mixtures of compounds from different classes is widely accepted as optimal resistance management. However, this strategy may promote the evolution of more generalist resistance mechanisms. Here we test this hypothesis at a national-scale in an economically important agricultural weed: blackgrass (Alopecurus myosuroides), for which herbicide resistance is a major economic issue. Our results reveal that greater use of herbicide mixtures is associated with lower levels of specialist resistance mechanisms, but higher levels of a generalist mechanism implicated in enhanced metabolism of herbicides with diverse modes of action. Our results indicate a potential evolutionary trade-off in resistance management, whereby attempts to reduce selection for specialist resistance traits may promote the evolution of generalist resistance. We contend that where specialist and generalist resistance mechanisms co-occur, similar trade-offs will be evident, calling into question the ubiquity of resistance management based on mixtures and combination therapies

Small-scale and regional spatial dynamics of an annual plant with contrasting sexual systems

Plant demography is known to depend on both spatial dynamics and life history, but how these two factors interact is poorly understood. We conducted a longitudinal study of the wind-pollinated annual plant Mercurialis annua that varies geographically in its sexual system to investigate this interaction. Metapopulation demographic models predict that regular population turnover should be a more common feature of monomorphic than dimorphic populations because males and females cannot found new populations by selfing but hermaphrodites can. We tested the prediction that rates of population turnover would be higher in monomorphic compared to dimorphic regions. We surveyed 356 populations of M. annua along five regional transects in Morocco and the Iberian Peninsula over a 3-year period to examine their demography and persistence. Each transect crossed a transition in the sexual system, from a monomorphic region where almost all populations were hermaphroditic to a dimorphic one in which most populations had separate sexes (males with females or hermaphrodites). As predicted, rates of local apparent extinctions (i.e., the disappearance of adult plants) were nearly 50% higher in monomorphic compared to dimorphic regions. Local extinctions appeared to be driven by changes in vegetation cover, with extinctions tending to occur in sites in which perennial cover also declined. This suggests that disturbance is a primary agent of local extinctions. We further examined the influence of regional dynamics on local demographic properties by investigating patterns of spatial autocorrelation in population density across years. We found positive spatial autocorrelations in plant densities within regions for both sexual systems. However, these positive autocorrelations extended over shorter distances in monomorphic regions, perhaps as a result of greater population flux in these regions. Synthesis. Our study shows that population dynamics may be influenced by processes acting at a range of spatial scales: within patches, across patches within sites, and across sites within regions, as well as by life-history variation. In Mercurialis annua, regional variation in apparent extinction rates is affected by life history and implicated in regulating the geographical distribution of populations with different sexual systems

Mapping the drivers of parasitic weed abundance at a national scale : a new approach applied to Striga asiatica in the mid‐west of Madagascar

The parasitic weed genus Striga causes huge losses to crop production in sub‐Saharan Africa, estimated to be in excess of $7 billion per year. There is a paucity of reliable distribution data for Striga ; however, such data are urgently needed to understand current drivers, better target control efforts, as well as to predict future risks. To address this, we developed a methodology to enable rapid, large‐scale monitoring of Striga populations. We used this approach to uncover the factors that currently drive the abundance and distribution of Striga asiatica in Madagascar. Two long‐distance transects were established across the middle‐west region of Madagascar in which S. asiatica abundance in fields adjacent to the road was estimated. Management, crop structure and soil data were also collected. Analysis of the data suggests that crop variety, companion crop and previous crop were correlated with Striga density. A positive relationship between within‐field Striga density and the density of the nearest neighbouring fields indicates that spatial configuration and connectivity of suitable habitats is also important in determining Striga spread. Our results demonstrate that we are able to capture distribution and management data for Striga density at a landscape scale and use this to understand the ecological and agronomic drivers of abundance. The importance of crop varieties and cropping patterns is significant, as these are key socio‐economic elements of Malagasy cropping practices. Therefore, they have the potential to be promoted as readily available control options, rather than novel technologies requiring introduction

Effects of habitat and land use on breeding season density of male Asian Houbara Chlamydotis macqueenii

Landscape-scale habitat and land-use influences on Asian Houbara Chlamydotis macqueenii (IUCN Vulnerable) remain unstudied, while estimating numbers of this cryptic, low-density, over-hunted species is challenging. In spring 2013, male houbara were recorded at 231 point counts, conducted twice, across a gradient of sheep density and shrub assemblages within 14,300 km² of the Kyzylkum Desert, Uzbekistan. Four sets of models related male abundance to: (1) vegetation structure (shrub height and substrate); (2) shrub assemblage; (3) shrub species composition (multidimensional scaling); (4) remote-sensed derived land-cover (GLOBCOVER, 4 variables). Each set also incorporated measures of landscape rugosity and sheep density. For each set, multi-model inference was applied to generalised linear mixed models of visit-specific counts that included important detectability covariates and point ID as a random effect. Vegetation structure received strongest support, followed by shrub species composition and shrub assemblage, with weakest support for the GLOBCOVER model set. Male houbara numbers were greater with lower mean shrub height, more gravel and flatter surfaces, but were unaffected by sheep density. Male density (mean 0.14 km-2, 95% CI, 0.12‒0.15) estimated by distance analysis differed substantially among shrub assemblages, being highest in vegetation dominated by Salsola rigida (0.22 [CI, 0.20‒0.25]), high in areas of S. arbuscula and Astragalus (0.14 [CI, 0.13‒0.16] and 0.15 [CI, 0.14‒0.17] respectively), lower (0.09 [CI, 0.08‒0.10]) in Artemisia and lowest (0.04 [CI, 0.04‒0.05]) in Calligonum. The study area was estimated to hold 1,824 males (CI: 1,645‒2,030). The spatial distribution of relative male houbara abundance, predicted from vegetation structure models, had the strongest correspondence with observed numbers in both model-calibration and the subsequent year’s data. We found no effect of pastoralism on male distribution but potential effects on nesting females are unknown. Density differences among shrub communities suggest extrapolation to estimate country- or range-wide population size must take account of vegetation composition

Quantification of CO2 removal in a large-scale enhanced weathering field trial on an oil palm plantation in Sabah, Malaysia

Modeling studies show that large-scale deployment of enhanced rock weathering on croplands has the potential to reduce levels of atmospheric carbon dioxide by the end of the century. There is, however, a pressing need to verify model predictions through long-term field trials. Here we report results from the first 3 years of an ongoing enhanced weathering field trial, carried out on an oil palm plantation in Sabah, Malaysia. Crushed silicate rock was applied to three hydrologically isolated catchments, and three adjacent (paired) reference catchments were left untreated. The drawdown of atmospheric CO2 was quantified via the export of alkalinity in stream waters and changes in soil carbonate content. The amended and reference catchments were found to have a similar extent of CO2 drawdown via alkalinity export [respectively, 3.8 ± 0.8 (1 SD) and 3.7 ± 0.6 (1 SD) tCO2 ha−1] when all catchments were averaged over the study period (October 2018 to July 2021). However, differences were observed between the different catchment pairs (plots): two of the plots displayed a similar extent of CO2 removal for both the amended and reference catchments, but the third amended catchment had a higher extent of CO2 removal of ~1 tCO2 ha−1 relative to its adjacent reference catchment. The difference in CO2 removal rates determined for this plot can likely be attributed to increased weathering of silicate minerals in the amended catchment. Soil carbonate concentrations were on average < 0.2 wt% CaCO3, but we report a small increase of ~0.03 wt% CaCO3 in the top 30 cm of soil in the amended soils relative to the reference catchments. The magnitude of CO2 drawdown via alkalinity export determined for these agricultural catchments is around an order of magnitude higher than in natural forested catchments in Sabah and similar to that of basaltic catchments. We show that these high weathering rates are primarily driven by weathering of carbonate fertilizers. The data presented from this field trial provide vital contextual information on the real-world efficacy and practicalities associated with the implementation of enhanced weathering for atmospheric CO2 removal that will help to inform further trials as well as wider-scale deployment

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change