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.

Oceanographic features and limited dispersal shape the population genetic structure of the vase sponge Ircinia campana in the Greater Caribbean.

Understanding population genetic structure can help us to infer dispersal patterns, predict population resilience and design effective management strategies. For sessile species with limited dispersal, this is especially pertinent because genetic diversity and connectivity are key aspects of their resilience to environmental stressors. Here, we describe the population structure of Ircinia campana, a common Caribbean sponge subject to mass mortalities and disease. Microsatellites were used to genotype 440 individuals from 19 sites throughout the Greater Caribbean. We found strong genetic structure across the region, and significant isolation by distance across the Lesser Antilles, highlighting the influence of limited larval dispersal. We also observed spatial genetic structure patterns congruent with oceanography. This includes evidence of connectivity between sponges in the Florida Keys and the southeast coast of the United States (>700 km away) where the oceanographic environment is dominated by the strong Florida Current. Conversely, the population in southern Belize was strongly differentiated from all other sites, consistent with the presence of dispersal-limiting oceanographic features, including the Gulf of Honduras gyre. At smaller spatial scales (<100 km), sites showed heterogeneous patterns of low-level but significant genetic differentiation (chaotic genetic patchiness), indicative of temporal variability in recruitment or local selective pressures. Genetic diversity was similar across sites, but there was evidence of a genetic bottleneck at one site in Florida where past mass mortalities have occurred. These findings underscore the relationship between regional oceanography and weak larval dispersal in explaining population genetic patterns, and could inform conservation management of the species.

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.

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.

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.

Host genetics and geography influence microbiome composition in the sponge Ircinia campana.

Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome. Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome. We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing. We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location. Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco-evolutionary dynamics of host-associated microbiomes.

Know Your Monkey: Identifying Primate Conservation Challenges in an Indigenous Kichwa Community Using an Ethnoprimatological Approach.

Increasing pressure on tropical forests is continually highlighting the need to find new solutions that mitigate the impact of human populations on biodiversity. However, developing solutions that can tackle the drivers of anthropogenic pressure, or at least take them into account, hinges upon building a good understanding of the culture and perceptions of local people. This study aims to provide an overview of the ethnoprimatology of an indigenous Kichwa community in the Ecuadorian Amazon that maintains a traditional lifestyle but also has good access to markets. We examine whether primates are seen as a distinctive group and their relative importance as sources of bushmeat and as household pets. Pile-sorting exercises revealed that although locals generally group members of the order Primates together, tree-dwelling non-primates including sloths, coatis, kinkajous and tamanduas are also frequently classified as 'monkeys'. The perceived importance of primates to the forest and the community lay more in their potential as bushmeat, and only 1 respondent identified an ecological role for the group in terms of seed dispersal. Gaining a better understanding of local perceptions will allow for better-informed conservation decisions that are more aware of potential impacts and are more likely to gain community support.

Amphibian Symbiotic Bacteria Do Not Show a Universal Ability To Inhibit Growth of the Global Panzootic Lineage of Batrachochytrium dendrobatidis.

Microbiomes associated with multicellular organisms influence the disease susceptibility of hosts. The potential exists for such bacteria to protect wildlife from infectious diseases, particularly in the case of the globally distributed and highly virulent fungal pathogen Batrachochytrium dendrobatidis of the global panzootic lineage (B. dendrobatidis GPL), responsible for mass extinctions and population declines of amphibians. B. dendrobatidis GPL exhibits wide genotypic and virulence variation, and the ability of candidate probiotics to restrict growth across B. dendrobatidis isolates has not previously been considered. Here we show that only a small proportion of candidate probiotics exhibited broad-spectrum inhibition across B. dendrobatidis GPL isolates. Moreover, some bacterial genera showed significantly greater inhibition than others, but overall, genus and species were not particularly reliable predictors of inhibitory capabilities. These findings indicate that bacterial consortia are likely to offer a more stable and effective approach to probiotics, particularly if related bacteria are selected from genera with greater antimicrobial capabilities. Together these results highlight a complex interaction between pathogens and host-associated symbiotic bacteria that will require consideration in the development of bacterial probiotics for wildlife conservation. Future efforts to construct protective microbiomes should incorporate bacteria that exhibit broad-spectrum inhibition of B. dendrobatidis GPL isolates.

Tagging frogs with passive integrated transponders causes disruption of the cutaneous bacterial community and proliferation of opportunistic fungi.

Symbiotic bacterial communities play a key role in protecting amphibians from infectious diseases including chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis. Events that lead to the disruption of the bacterial community may have implications for the susceptibility of amphibians to such diseases. Amphibians are often marked both in the wild and in captivity for a variety of reasons, and although existing literature indicates that marking techniques have few negative effects, the response of cutaneous microbial communities has not yet been investigated. Here we determine the effects of passive integrated transponder (PIT) tagging on culturable cutaneous microbial communities of captive Morelet's tree frogs (Agalychnis moreletii) and assess the isolated bacterial strains for anti-B. dendrobatidis activity in vitro. We find that PIT tagging causes a major disruption to the bacterial community associated with the skin of frogs (∼12-fold increase in abundance), as well as a concurrent proliferation in resident fungi (up to ∼200-fold increase). Handling also caused a disruption the bacterial community, although to a lesser extent than PIT tagging. However, the effects of both tagging and handling were temporary, and after 2 weeks, the bacterial communities were similar to their original compositions. We also identify two bacterial strains that inhibit B. dendrobatidis, one of which increased in abundance on PIT-tagged frogs at 1 day postmarking, while the other was unaffected. These results show that PIT tagging has previously unobserved consequences for cutaneous microbial communities of frogs and may be particularly relevant for studies that intend to use PIT tagging to identify individuals involved in trials to develop probiotic treatments.

Parasitoid wasps influence where aphids die via an interspecific indirect genetic effect.

Host-parasite interactions are a key paradigm for understanding the process of coevolution. Central to coevolution is how genetic variation in interacting species allows parasites to evolve manipulative strategies. However, genetic variation in the parasite may also be associated with host phenotype changes, thereby changing the selection on both species. For instance, parasites often induce changes in the behaviour of their host to maximize their own fitness, yet the quantitative genetic basis for behavioural manipulation has not been fully demonstrated. Here, we show that the genotype of the parasitoid wasp Aphidius ervi has a significant effect on where its aphid host Acyrthosiphon pisum moves to die following parasitism, including the likelihood that the aphid abandons the plant. These results provide a clear example of an interspecific indirect genetic effect whereby the genetics of one species influences the expression of a specific behavioural trait in another.

A minute fossil phoretic mite recovered by phase-contrast X-ray computed tomography.

High-resolution phase-contrast X-ray computed tomography (CT) reveals the phoretic deutonymph of a fossil astigmatid mite (Acariformes: Astigmata) attached to a spider's carapace (Araneae: Dysderidae) in Eocene (44-49 Myr ago) Baltic amber. Details of appendages and a sucker plate were resolved, and the resulting three-dimensional model demonstrates the potential of tomography to recover morphological characters of systematic significance from even the tiniest amber inclusions without the need for a synchrotron. Astigmatids have an extremely sparse palaeontological record. We confirm one of the few convincing fossils, potentially the oldest record of Histiostomatidae. At 176 µm long, we believe this to be the smallest arthropod in amber to be CT-scanned as a complete body fossil, extending the boundaries for what can be recovered using this technique. We also demonstrate a minimum age for the evolution of phoretic behaviour among their deutonymphs, an ecological trait used by extant species to disperse into favourable environments. The occurrence of the fossil on a spider is noteworthy, as modern histiostomatids tend to favour other arthropods as carriers.

Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropical forest ecosystem.

Within the area of community genetics there is an expanding volume of literature demonstrating how within-species genetic variation in temperate trees can have important effects on structuring animal and plant communities. The influence of intraspecific genetic variation on associated communities in relatively more complex ecosystems is only starting to be appreciated. Within tropical forests, epiphytic bromeliad plants often grow high in the canopy and create unique nutrient-rich microhabitats on which many invertebrate and vertebrate species depend. We investigated the influence of within-species genetic variation in the bromeliad Aechmea bracteata on the invertebrate microhabitat community. We found that more genetically similar bromeliad plants were host to more similar communities of juvenile-stage invertebrates, but not adult invertebrates. We discuss possible mechanisms for this, including differential survival and active female oviposition choice. Our work shows that the impact of within-species genetic variation on associated ecological communities may be more general than previously considered. These results agree with recent research suggesting that within-species genetic variation may perform a supporting ecosystem service for maintaining community and ecological processes.

Differences in carotenoid accumulation among three feeder-cricket species: implications for carotenoid delivery to captive insectivores.

There are a limited number of feeder-invertebrates available to feed captive insectivores, and many are deficient in certain nutrients. Gut-loading is used to increase the diversity of nutrients present in the captive insectivore diet; however, little is known about delivery of carotenoids via gut-loading. Carotenoids may influence health and reproduction due to their roles in immune and antioxidant systems. We assessed interspecific variation in carotenoid accumulation and retention in three feeder-cricket species (Gryllus bimaculatus, Gryllodes sigillatus and Acheta domesticus) fed one of three diets (wheat-bran, fish-food based formulated diet, and fresh fruit and vegetables). Out of the three species of feeder-cricket in the fish-food-based dietary treatment group, G. bimaculatus had the greatest total carotenoid concentration. All cricket species fed the wheat-bran diet had very low carotenoid concentrations. Species on the fish-food-based diet had intermediate carotenoid concentrations, and those on the fruit and vegetable diet had the highest concentrations. Carotenoid retention was poor across all species. Overall, this study shows that, by providing captive insectivores with G. bimaculatus crickets recently fed a carotenoid-rich diet, the quantity of carotenoids in the diet can be increased.

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.

The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs.

Environmental degradation has the potential to alter key mutualisms that underlie the structure and function of ecological communities. How microbial communities associated with fishes vary across populations and in relation to habitat characteristics remains largely unknown despite their fundamental roles in host nutrition and immunity. We find significant differences in the gut microbiome composition of a facultative coral-feeding butterflyfish (Chaetodon capistratus) across Caribbean reefs that differ markedly in live coral cover (∼0-30%). Fish gut microbiomes were significantly more variable at degraded reefs, a pattern driven by changes in the relative abundance of the most common taxa potentially associated with stress. We also demonstrate that fish gut microbiomes on severely degraded reefs have a lower abundance of Endozoicomonas and a higher diversity of anaerobic fermentative bacteria, which may suggest a less coral dominated diet. The observed shifts in fish gut bacterial communities across the habitat gradient extend to a small set of potentially beneficial host associated bacteria (i.e., the core microbiome) suggesting essential fish-microbiome interactions may be vulnerable to severe coral degradation.

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.

Computed tomography recovers data from historical amber: an example from huntsman spiders.

Computed tomography (CT) methods were applied to a problematic fossil spider (Arachnida: Araneae) from the historical Berendt collection of Eocene (ca. 44-49 Ma) Baltic amber. The original specimens of Ocypete crassipes Koch and Berendt 1854 are in dark, oxidised amber and the published descriptions lack detail. Despite this, they were subsequently assigned to the living Pantropical genus Heteropoda Latreille, 1804 and are ostensibly the oldest records of huntsman spiders (Sparassidae) in general. Given their normally large size, and presumptive ability to free themselves more easily from resin, it would be surprising to find a sparassid in amber and traditional (optical) methods of study would likely have left O. crassipes as an equivocal record--probably a nomen dubium. However, phase contrast enhanced X-ray CT revealed exquisite morphological detail and thus 'saved' this historical name by revealing characters which confirm that it's a bona fide member both of Sparassidae and the subfamily Eusparassinae. We demonstrate here that CT studies facilitate taxonomic equivalence even between recent spiders and unpromising fossils described in older monographs. In our case, fine structural details such as eye arrangement, cheliceral dentition, and leg characters like a trilobate membrane, spination and claws, allow a precise referral of this fossil to an extant genus as Eusparassus crassipes (Koch and Berendt 1854) comb. nov.

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.

Community genetic interactions mediate indirect ecological effects between a parasitoid wasp and rhizobacteria.

Indirect ecological effects (IEEs) clearly influence species dynamics and abundance, yet relatively little is known about how they influence the evolution of species involved. While genetic variation in the species causing and responding to the IEE has obvious effects, the influence of genetic variation in intermediate species remains unexamined. Given the often counterintuitive responses of populations to IEEs this seems a significant omission. Following a community genetics approach, we used a model tetra-trophic system (parasitoid wasp, aphid, barley, and rhizobacteria) to investigate the effect of genetic interactions within the two linking species (aphids and barley) on the IEE of rhizobacteria on wasps. We show that 12.4% of the variation in wasp size, a proxy for fitness, is explained by higher-order interactions between aphid genotype (A), barley genotype (B), and presence or absence of rhizobacteria (R) (Genotype[B] x Genotype[A] x Environment[R]). Thus, the IEE of rhizobacteria on the parasitoid wasp is influenced by the specific combination of aphid and barley genotypes that mediate the interactions. In some cases changes in the genotypes of the intermediate species completely reverse the effect of rhizobacteria on wasp size. Our work demonstrates that within-species genetic variation is important in shaping IEEs in communities, an essential component of community evolutionary processes.

Understanding the lessons and limitations of conservation and development.

The lack of concrete instances in which conservation and development have been successfully merged has strengthened arguments for strict exclusionist conservation policies. Research has focused more on social cooperation and conflict of different management regimes and less on how these factors actually affect the natural environments they seek to conserve. Consequently, it is still unknown which strategies yield better conservation outcomes? We conducted a meta-analysis of 116 published case studies on common resource management regimes from Africa, south and central America, and southern and Southeast Asia. Using ranked sociodemographic, political, and ecological data, we analyzed the effect of land tenure, population size, social heterogeneity, as well as internally devised resource-management rules and regulations (institutions) on conservation outcome. Although land tenure, population size, and social heterogeneity did not significantly affect conservation outcome, institutions were positively associated with better conservation outcomes. There was also a significant interaction effect between population size and institutions, which implies complex relationships between population size and conservation outcome. Our results suggest that communities managing a common resource can play a significant role in conservation and that institutions lead to management regimes with lower environmental impacts.