Complex urban environments provide Apis mellifera with a richer plant forage than suburban and more rural landscapes.

Growth in the global development of cities, and increasing public interest in beekeeping, has led to increase in the numbers of urban apiaries. Towns and cities can provide an excellent diet for managed bees, with a diverse range of nectar and pollen available throughout a long flowering season, and are often more ecologically diverse than the surrounding rural environments. Accessible urban honeybee hives are a valuable research resource to gain insights into the diet and ecology of wild pollinators in urban settings. We used DNA metabarcoding of the rbcL and ITS2 gene regions to characterize the pollen community in Apis mellifera honey, inferring the floral diet, from 14 hives across an urban gradient around Greater Manchester, UK. We found that the proportion of urban land around a hive is significantly associated with an increase in the diversity of plants foraged and that invasive and non-native plants appear to play a critical role in the sustenance of urban bees, alongside native plant species. The proportion of improved grassland, typical of suburban lawns and livestock farms, is significantly associated with decreases in the diversity of plant pollen found in honey samples. These findings are relevant to urban landscape developers motivated to encourage biodiversity and bee persistence, in line with global bio-food security agendas.

Genetic diversity of honeybee colonies predicts gut bacterial diversity of individual colony members.

The gut microbiota of social bees is relatively simple and dominated by a set of core taxa found consistently in individuals around the world. Yet, variation remains and can affect host health. We characterized individual- and regional-scale variation in honeybee (Apis mellifera) gut microbiota from 64 colonies in North-West England by sequencing the V4 region of the 16S rRNA gene and asked whether microbiota were influenced by host genotype and landscape composition. We also characterized the genotypes of individual bees and the land cover surrounding each colony. The literature-defined core taxa dominated across the region despite the varied environments. However, there was variation in the relative abundance of core taxa, and colony membership explained much of this variation. Individuals from more genetically diverse colonies had more diverse microbiotas, but individual genetic diversity did not influence gut microbial diversity. There were weak trends for colonies in more similar landscapes to have more similar microbiota, and for bees from more urban landscapes to have less diverse microbiota. To our knowledge, this is the first report for any species that the gut bacterial communities of individuals are influenced by the genotypes of others in the population.

Mangrove diversity is more than fringe deep.

Mangroves form coastal tropical forests in the intertidal zone and are an important component of shoreline protection. In comparison to other tropical forests, mangrove stands are thought to have relatively low genetic diversity with population genetic structure gradually increasing with distance along a coastline. We conducted genetic analyses of mangrove forests across a range of spatial scales; within a 400 m2 parcel comprising 181 Rhizophora mangle (red mangrove) trees, and across four sites ranging from 6-115 km apart in Honduras. In total, we successfully genotyped 269 R. mangle trees, using a panel of 677 SNPs developed with 2b-RAD methodology. Within the 400 m2 parcel, we found two distinct clusters with high levels of genetic differentiation (FST = 0.355), corresponding to trees primarily located on the seaward fringe and trees growing deeper into the forest. In contrast, there was limited genetic differentiation (FST = 0.027-0.105) across the sites at a larger scale, which had been predominantly sampled along the seaward fringe. Within the 400 m2 parcel, the cluster closest to the seaward fringe exhibited low genetic differentiation (FST = 0.014-0.043) with the other Honduran sites, but the cluster further into the forest was highly differentiated from them (FST = 0.326-0.414). These findings contradict the perception that genetic structure within mangroves forests occurs mainly along a coastline and highlights that there is greater genetic structure at fine spatial scales.

Evidence for the genetic similarity rule at an expanding mangrove range limit.

PREMISE: Host-plant genetic variation can shape associated communities of organisms. These community-genetic effects include (1) genetically similar hosts harboring similar associated communities (i.e., the genetic similarity rule) and (2) host-plant heterozygosity increasing associated community diversity. Community-genetic effects are predicted to be less prominent in plant systems with limited genetic variation, such as those at distributional range limits. Yet, empirical evidence from such systems is limited. METHODS: We sampled a natural population of a mangrove foundation species (Avicennia germinans) at an expanding range limit in Florida, USA. We measured genetic variation within and among 40 host trees with 24 nuclear microsatellite loci and characterized their foliar endophytic fungal communities with internal transcribed spacer (ITS1) gene amplicon sequencing. We evaluated relationships among host-tree genetic variation, host-tree spatial location, and the associated fungal communities. RESULTS: Genetic diversity was low across all host trees (mean: 2.6 alleles per locus) and associated fungal communities were relatively homogeneous (five sequence variants represented 78% of all reads). We found (1) genetically similar host trees harbored similar fungal communities, with no detectable effect of interhost geographic distance. (2) Host-tree heterozygosity had no detectable effect, while host-tree absolute spatial location affected community alpha diversity. CONCLUSIONS: This research supports the genetic similarity rule within a range limit population and helps broaden the current scope of community genetics theory by demonstrating that community-genetic effects can occur even at expanding distributional limits where host-plant genetic variation may be limited. Our findings also provide the first documentation of community-genetic effects in a natural mangrove system.

Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome.

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

Genetic structure of a remnant Acropora cervicornis population.

Amongst the global decline of coral reefs, hope spots such as Cordelia Bank in Honduras, have been identified. This site contains dense, remnant thickets of the endangered species Acropora cervicornis, which local managers and conservation organizations view as a potential source population for coral restoration projects. The aim of this study was to determine the genetic diversity of colonies across three banks within the protected area. We identified low genetic diversity (FST = 0.02) across the three banks, and genetic similarity of colonies ranged from 91.3 to 95.8% between the banks. Clonality rates were approximately 30% across the three banks, however, each genotype identified was unique to each bank. Despite the low genetic diversity, subtle genetic differences within and among banks were demonstrated, and these dense thickets were shown not to be comprised of a single or a few genotypes. The presence of multiple genotypes suggests A. cervicornis colonies from these banks could be used to maintain and enhance genetic diversity in restoration projects. Management of hope spots, such as Cordelia Bank, and the incorporation of genetic information into restoration projects to ensure genetic diversity within out-planted populations, will be critical in the ongoing challenge of conserving and preserving coral reefs.

Characterizing the genetic diversity of the Andean blueberry (Vaccinium floribundum Kunth.) across the Ecuadorian Highlands.

The Ecuadorian páramo, a high altitude tundra-like ecosystem, is a unique source of various ecosystem services and distinct biodiversity. Anthropogenic activities are associated with its fragmentation, which alters ecological factors and directly threatens resident species. Vaccinium floribundum Kunth., commonly known as Andean blueberry or mortiño, is a wild shrub endemic to the Andean region and highly valued in Ecuador for its berries, which are widely used in food preparations and hold an important cultural value. Since it is a wild species, mortiño could be vulnerable to environmental changes, resulting in a reduction of the size and distribution of its populations. To evaluate the extent of these effects on the mortiño populations, we assessed the genetic diversity and population structure of the species along the Ecuadorian highlands. We designed and developed a set of 30 species-specific SSR (simple sequence repeats) markers and used 16 of these to characterize 100 mortiño individuals from 27 collection sites. Our results revealed a high degree of genetic diversity (HE = 0.73) for the Ecuadorian mortiño, and a population structure analyses suggested the existence of distinct genetic clusters present in the northern, central and southern highlands. A fourth, clearly differentiated cluster was also found and included individuals from locations at higher elevations. We suggest that the population structure of the species could be explained by an isolation-by-distance model and can be associated with the geological history of the Andean region. Our results suggest that elevation could also be a key factor in the differentiation of mortiño populations. This study provides an extensive overview of the species across its distribution range in Ecuador, contributing to a better understanding of its conservation status. These results can assist in the development of conservation programs for this valuable biological and cultural resource and for the páramo ecosystem as a whole.

Hurricanes overcome migration lag and shape intraspecific genetic variation beyond a poleward mangrove range limit.

Expansion of many tree species lags behind climate change projections. Extreme storms can rapidly overcome this lag, especially for coastal species, but how will storm-driven expansion shape intraspecific genetic variation? Do storms provide recruits only from the nearest sources, or from more distant sources? Answers to these questions have ecological and evolutionary implications, but empirical evidence is absent from the literature. In 2017, Hurricane Irma provided an opportunity to address this knowledge gap at the northern range limit of the neotropical black mangrove (Avicennia germinans) on the Atlantic coast of Florida, USA. We observed massive post-hurricane increases in beach-stranded A. germinans propagules at, and past, this species' present day range margin when compared to a previously surveyed nonhurricane year. Yet, propagule dispersal does not guarantee subsequent establishment and reproductive success (i.e., effective dispersal). We also evaluated prior effective dispersal along this coastline with isolated A. germinans trees identified beyond the most northern established population. We used 12 nuclear microsatellite loci to genotype 896 hurricane-driven drift propagules from nine sites and 10 isolated trees from four sites, determined their sources of origin, and estimated dispersal distances. Almost all drift propagules and all isolated trees came from the nearest sources. This research suggests that hurricanes are a prerequisite for poleward range expansion of a coastal tree species and that storms can shape the expanding gene pool by providing almost exclusively range-margin genotypes. These insights and empirical estimates of hurricane-driven dispersal distances should improve our ability to forecast distributional shifts of coastal species.

Mangroves give cause for conservation optimism, for now.

Friess et al. discuss the results of conservation efforts for mangrove forests in recent years.

Blind Trading: A Literature Review of Research Addressing the Welfare of Ball Pythons in the Exotic Pet Trade.

Extensive numbers of Ball pythons are caught, bred, traded and subsequently kept in captivity across the world as part of the exotic pet industry. Despite their widespread availability as pets, relatively little is known about the potential welfare challenges affecting them. We reviewed the literature for research focused on the health and welfare of Ball pythons in the international pet trade. From a total of 88 articles returned from the search criteria, our analysis showed that very few actually focused on trade (10%) or animal welfare (17%). Instead, the majority (64%) of articles focused on veterinary science. There was a considerable bias towards physical health, with most studies neglecting the four other domains of animal welfare (behaviour, nutrition, environment and mental health). Furthermore, very few studies considered Ball pythons prior to resulting pet ownership, during wild capture and transportation or captive breeding operations. Our review demonstrates that our current understanding of welfare for Ball pythons traded as exotic pets is limited. We recommend that future research should focus on aspects of the industry that are currently overlooked, including the potential consequences of genetic selection during captive-breeding and the conditions provided for snakes prior to and during international transportation.

Is the central-marginal hypothesis a general rule? Evidence from three distributions of an expanding mangrove species, Avicennia germinans (L.) L.

The central-marginal hypothesis (CMH) posits that range margins exhibit less genetic diversity and greater inter-population genetic differentiation compared to range cores. CMH predictions are based on long-held "abundant-centre" assumptions of a decline in ecological conditions and abundances towards range margins. Although much empirical research has confirmed CMH, exceptions remain almost as common. We contend that mangroves provide a model system to test CMH that alleviates common confounding factors and may help clarify this lack of consensus. Here, we document changes in black mangrove (Avicennia germinans) population genetics with 12 nuclear microsatellite loci along three replicate coastlines in the United States (only two of three conform to underlying "abundant-centre" assumptions). We then test an implicit prediction of CMH (reduced genetic diversity may constrain adaptation at range margins) by measuring functional traits of leaves associated with cold tolerance, the climatic factor that controls these mangrove distributional limits. CMH predictions were confirmed only along the coastlines that conform to "abundant-centre" assumptions and, in contrast to theory, range margin A. germinans exhibited functional traits consistent with greater cold tolerance compared to range cores. These findings support previous accounts that CMH may not be a general rule across species and that reduced neutral genetic diversity at range margins may not be a constraint to shifts in functional trait variation along climatic gradients.

Effects of maternal genotypic identity and genetic diversity of the red mangrove Rhizophora mangle on associated soil bacterial communities: A field-based experiment.

Loss of plant biodiversity can result in reduced abundance and diversity of associated species with implications for ecosystem functioning. In ecosystems low in plant species diversity, such as Neotropical mangrove forests, it is thought that genetic diversity within the dominant plant species could play an important role in shaping associated communities. Here, we used a manipulative field experiment to study the effects of maternal genotypic identity and genetic diversity of the red mangrove Rhizophora mangle on the composition and richness of associated soil bacterial communities. Using terminal restriction fragment length polymorphism (T-RFLP) community fingerprinting, we found that bacterial community composition differed among R. mangle maternal genotypes but not with genetic diversity. Bacterial taxa richness, total soil nitrogen, and total soil carbon were not significantly affected by maternal genotypic identity or genetic diversity of R. mangle. Our findings show that genotype selection in reforestation projects could influence soil bacterial community composition. Further research is needed to determine what impact these bacterial community differences might have on ecosystem processes, such as carbon and nitrogen cycling.

Multi-individual microsatellite identification: A multiple genome approach to microsatellite design (MiMi).

Bespoke microsatellite marker panels are increasingly affordable and tractable to researchers and conservationists. The rate of microsatellite discovery is very high within a shotgun genomic data set, but extensive laboratory testing of markers is required for confirmation of amplification and polymorphism. By incorporating shotgun next-generation sequencing data sets from multiple individuals of the same species, we have developed a new method for the optimal design of microsatellite markers. This new tool allows us to increase the rate at which suitable candidate markers are selected by 58% in direct comparisons and facilitate an estimated 16% reduction in costs associated with producing a novel microsatellite panel. Our method enables the visualisation of each microsatellite locus in a multiple sequence alignment allowing several important quality checks to be made. Polymorphic loci can be identified and prioritised. Loci containing fragment-length-altering mutations in the flanking regions, which may invalidate assumptions regarding the model of evolution underlying variation at the microsatellite, can be avoided. Priming regions containing point mutations can be detected and avoided, helping to reduce sample-site-marker specificity arising from genetic isolation, and the likelihood of null alleles occurring. We demonstrate the utility of this new approach in two species: an echinoderm and a bird. Our method makes a valuable contribution towards minimising genotyping errors and reducing costs associated with developing a novel marker panel. The Python script to perform our method of multi-individual microsatellite identification (MiMi) is freely available from GitHub (https://github.com/graemefox/mimi).

Cultivar Differences and Impact of Plant-Plant Competition on Temporal Patterns of Nitrogen and Biomass Accumulation.

Current niche models cannot explain multi-species plant coexistence in complex ecosystems. One overlooked explanatory factor is within-growing season temporal dynamism of resource capture by plants. However, the timing and rate of resource capture are themselves likely to be mediated by plant-plant competition. This study used Barley (Hordeum sp.) as a model species to examine the impacts of intra-specific competition, specifically inter- and intra-cultivar competition on the temporal dynamics of resource capture. Nitrogen and biomass accumulation of an early and late cultivar grown in isolation, inter- or intra- cultivar competition were investigated using sequential harvests. We did not find changes in the temporal dynamics of biomass accumulation in response to competition. However, peak nitrogen accumulation rate was significantly delayed for the late cultivar by 14.5 days and advanced in the early cultivar by 0.5 days when in intra-cultivar competition; there were no significant changes when in inter-cultivar competition. This may suggest a form of kin recognition as the target plants appeared to identify their neighbors and only responded temporally to intra-cultivar competition. The Relative Intensity Index found competition occurred in both the intra- and inter- cultivar mixtures, but a positive Land Equivalence Ratio value indicated complementarity in the inter-cultivar mixtures compared to intra-cultivar mixtures. The reason for this is unclear but may be due to the timing of the final harvest and may not be representative of the relationship between the competing plants. This study demonstrates neighbor-identity-specific changes in temporal dynamism in nutrient uptake. This contributes to our fundamental understanding of plant nutrient dynamics and plant-plant competition whilst having relevance to sustainable agriculture. Improved understanding of within-growing season temporal dynamism would also improve our understanding of coexistence in complex plant communities.

Temporal Dynamism of Resource Capture: A Missing Factor in Ecology?

Temporal dynamism of plant resource capture, and its impacts on plant-plant interactions, can have important regulatory roles in multispecies communities. For example, by modifying resource acquisition timing, plants might reduce competition and promote their coexistence. However, despite the potential wide ecological relevance of this topic, short-term (within growing season) temporal dynamism has been overlooked. This is partially a consequence of historic reliance on measures made at single points in time. We propose that with current technological advances this is a golden opportunity to study within growing season temporal dynamism of resource capture by plants in highly informative ways. We set out here an agenda for future developments in this research field, and explore how new technologies can deliver this agenda.

Detecting macroecological patterns in bacterial communities across independent studies of global soils.

The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential 'indicator' taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.

Biodiversity in agricultural landscapes: The effect of apple cultivar on epiphyte diversity.

In natural systems, extended phenotypes of trees can be important in determining the species composition and diversity of associated communities. Orchards are productive systems where trees dominate, and can be highly biodiverse, but few studies have considered the importance of tree genetic background in promoting associated biodiversity. We tested the effect of apple cultivar (plant genetic background) on the diversity and composition of the associated epiphytic bryophyte community across a total of seven cultivars in five productive East Anglian orchards where each orchard contained two cultivars. Data were collected from 617 individual trees, over 5 years. Species richness and community composition were significantly influenced by both orchard and cultivar. Differences among orchards explained 16% of the variation in bryophyte community data, while cultivar explained 4%. For 13 of the 41 bryophyte species recorded, apple cultivar was an important factor in explaining their distribution. While the effects of cultivar were small, we were able to detect them at multiple levels of analysis. We provide evidence that extended phenotypes act in productive as well as natural systems. With issues of food security ranking high on the international agenda, it is important to understand the impact of production regimes on associated biodiversity. Our results can inform mitigation of this potential conflict.

Interactions between the Bumblebee Bombus pascuorum and Red Clover (Trifolium pratense) Are Mediated by Plant Genetic Background.

Wildflower mixes are often planted around field margins to provide forage for pollinators. Although seed for these mixtures is often wild-sourced, for species where agricultural cultivars are available, for example red clover (Trifolium pratense), cultivars can also be included. Previous evidence suggests that plant genetic background can have a strong influence on plant-arthropod interactions and therefore the provenance and genetic background of the plants included in wildflower mixes could impact plant-pollinator interactions. We tested the performance of five individual T. pratense cultivars against two commercially available wild-sourced T. pratense populations in terms of their ability to attract potential pollinator species (focusing on bumblebees) and their floral traits using greenhouse and garden experiments. The main bumblebee observed interacting with T. pratense was Bombus pascuorum and we found no difference in the absolute number of B. pascuorum visiting the cultivars or wild populations. However, we found variation among cultivars and between wild populations in their ability to attract bumblebees, which seems to be related to their relative investment in different floral traits. There was a positive relationship between biomass and number of inflorescences produced by the wild populations of T. pratense, which was not apparent for the cultivars. This suggests that artificial selection on the cultivars has changed the G-matrix of correlated traits. We show that agricultural cultivars of T. pratense can be as effective as wild populations at attracting pollinators such as bumblebees, but that the genetic background of both cultivars and wild populations can have a significant impact on the attractiveness of the plant to pollinators. We also show divergence in the correlated traits of T. pratense cultivars and wild populations that could lead to outbreeding depression if the plants interbreed.

The genetics of indirect ecological effects-plant parasites and aphid herbivores.

When parasitic plants and aphid herbivores share a host, both direct and indirect ecological effects (IEEs) can influence evolutionary processes. We used a hemiparasitic plant (Rhinanthus minor), a grass host (Hordeum vulgare) and a cereal aphid (Sitobion avenae) to investigate the genetics of IEEs between the aphid and the parasitic plant, and looked to see how these might affect or be influenced by the genetic diversity of the host plants. Survival of R. minor depended on the parasite's population of origin, the genotypes of the aphids sharing the host and the genetic diversity in the host plant community. Hence the indirect effects of the aphids on the parasitic plants depended on the genetic environment of the system. Here, we show that genetic variation can be important in determining the outcome of IEEs. Therefore, IEEs have the potential to influence evolutionary processes and the continuity of species interactions over time.

Host-plant genotypic diversity and community genetic interactions mediate aphid spatial distribution.

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three-species plant-aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi-parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host-plant community than in a genetic monoculture, with host-plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host-plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host-plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.