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Phylosymbiosis is an association between host-associated microbiome composition and host phylogeny. This pattern can arise via the evolution of host traits, habitat preferences, diets, and the co-diversification of hosts and microbes. Understanding the drivers of phylosymbiosis is vital for modelling disease-microbiome interactions and manipulating microbiomes in multi-host systems. This study quantifies phylosymbiosis in Appalachian salamander skin in the context of infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd), while accounting for environmental microbiome exposure. We sampled ten salamander species representing >150M years of divergence, assessed their Bd infection status, and analysed their skin and environmental microbiomes. Our results reveal a significant signal of phylosymbiosis, whereas the local environmental pool of microbes, climate, geography, and Bd infection load had a smaller impact. Host-microbe co-speciation was not evident, indicating that the effect stems from the evolution of host traits influencing microbiome assembly. Bd infection is correlated with host phylogeny and the abundance of Bd-inhibitory bacterial strains, suggesting that the long-term evolutionary dynamics between salamander hosts and their skin microbiomes affect the present-day distribution of the pathogen, along with habitat-linked exposure risk. Five Bd-inhibitory bacterial strains showed unusual generalism: occurring in most host species and habitats. These generalist strains may enhance the likelihood of probiotic manipulations colonising and persisting on hosts. Our results underscore the substantial influence of host-microbiome eco-evolutionary dynamics on environmental health and disease outcomes., (© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)

Background: Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species., Results: In this study on the obligate symbiosis between the gutless marine annelid Olavius algarvensis and its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80 O. algarvensis individuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of all O. algarvensis individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted., Conclusions: We hypothesize that variable degrees of fidelity are advantageous for O. algarvensis by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. Video Abstract., (© 2022. The Author(s).)

Background: Microbiomes can have profound impacts on host biology and evolution, but to date, remain vastly understudied in spiders despite their unique and diverse predatory adaptations. This study evaluates closely related species of spiders and their host-microbe relationships in the context of phylosymbiosis, an eco-evolutionary pattern where the microbial community profile parallels the phylogeny of closely related host species. Using 16S rRNA gene amplicon sequencing, we characterized the microbiomes of five species with known phylogenetic relationships from the family Theridiidae, including multiple closely related widow spiders (L. hesperus, L. mactans, L. geometricus, S. grossa, and P. tepidariorum)., Results: We compared whole animal and tissue-specific microbiomes (cephalothorax, fat bodies, venom glands, silk glands, and ovary) in the five species to better understand the relationship between spiders and their microbial symbionts. This showed a strong congruence of the microbiome beta-diversity of the whole spiders, cephalothorax, venom glands, and silk glands when compared to their host phylogeny. Our results support phylosymbiosis in these species and across their specialized tissues. The ovary tissue microbial dendrograms also parallel the widow phylogeny, suggesting vertical transfer of species-specific bacterial symbionts. By cross-validating with RNA sequencing data obtained from the venom glands, silk glands and ovaries of L. hesperus, L. geometricus, S. grossa, and P. tepidariorum we confirmed that several microbial symbionts of interest are viably active in the host., Conclusion: Together these results provide evidence that supports the importance of host-microbe interactions and the significant role microbial communities may play in the evolution and adaptation of their hosts.

Host-associated microbes facilitate diverse biotic and abiotic interactions between hosts and their environments. Experimental alterations of host-associated microbial communities frequently decrease host fitness, yet much less is known about if and how host-microbiome interactions are altered by natural perturbations, such as introduction events. Here, we begin to assess this question in Onthophagus dung beetles, a species-rich and geographically widely distributed genus whose members rely on vertically transmitted microbiota to support normal development. Specifically, we investigated to what extent microbiome community membership shifts during host introduction events and the relative significance of ancestral associations and novel environmental conditions in the structuring of microbial communities of introduced host species. Our results demonstrate that both evolutionary history and local environmental forces structure the microbial communities of these animals, but that their relative importance is shaped by the specific circumstances that characterize individual introduction events. Furthermore, we identify microbial taxa such as Dysgonomonas that may constitute members of the core Onthophagus microbiome regardless of host population or species, but also Wolbachia which associates with Onthophagus beetles in a species or even population-specific manner. We discuss the implications of our results for our understanding of the evolutionary ecology of symbiosis in dung beetles and beyond.

Mammalian gut microbiomes profoundly influence host fitness, but the processes that drive the evolution of host-microbiome systems are poorly understood. Recent studies suggest that mammals and their individual gut symbionts can have parallel evolutionary histories, as represented by their congruent phylogenies. These "co-phylogenetic" patterns are signatures of ancient co-speciation events and illustrate the cohesiveness of the mammalian host-gut microbiome entity over evolutionary times. Theory predicts that co-speciation between mammals and their gut symbionts could result from their co-evolution. However, there is only limited evidence of such co-evolution. Here, we propose a model that explains cophylogenetic patterns without relying on co-evolution. Specifically, we suggest that individual gut bacteria are likely to diverge in patterns recapitulating host phylogeny when hosts undergo allopatric speciation, limiting inter-host bacterial dispersal and genomic recombination. We provide evidence that the model is empirically grounded and propose a series of observational and experimental approaches to test its validity., Competing Interests: Declaration of Interests E.J.A. is a co-founder and shareholder of Finch Therapeutics, a company that specializes in microbiome-targeted therapeutics., (Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.)

Background: The vertebrate clade diverged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The divergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of diversity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize (1) the skin microbiome will be host and clade-specific, (2) evolutionary difference in elasmobranch and teleost will correspond with a concomitant increase in host-microbiome dissimilarity, and (3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes., Results: We show that the taxonomic and functional composition of the microbiomes is host-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch's average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes., Conclusion: Our results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest divergence of extant vertebrate hosts and reveals that microbial relationships are not consistent across evolutionary timescales. Video abstract.

In numerous animal clades, the evolutionary history of host species drives patterns of gut microbial community structure, resulting in more divergent microbiota with increasing phylogenetic distance between hosts. This phenomenon, termed phylosymbiosis, has been observed in diverse evolutionary lineages, but has been difficult to detect in birds. Previous tests of phylosymbiosis among birds have been conducted using wild individuals, and thus interspecific differences in diet and environment may have masked a phylogenetic signal. Therefore, we tested for phylosymbiosis among all 15 species of cranes (family Gruidae) housed in the same captive environment and maintained on identical diets. 16S rRNA sequencing revealed that crane species harbour distinct gut microbiota. Overall, we detected marginally significant patterns of phylosymbiosis, the strength of which was increased when including the estimates of absolute microbial abundance (rather than relative abundance) derived from microbial densities determined by flow cytometry. Using this approach, we detected the statistically significant signatures of phylosymbiosis only after removing male cranes from our analysis, suggesting that using mixed-sex animal cohorts may prevent the detection of phylosymbiosis. Though weak compared with mammals (and especially insects), these results provide evidence of phylosymbiosis in birds. We discuss the potential differences between birds and mammals, such as transmission routes and host filtering, that may underlie the differences in the strength of phylosymbiosis.

Phylosymbiosis was recently formulated to support a hypothesis-driven framework for the characterization of a new, cross-system trend in host-associated microbiomes. Defining phylosymbiosis as 'microbial community relationships that recapitulate the phylogeny of their host', we review the relevant literature and data in the last decade, emphasizing frequently used methods and regular patterns observed in analyses. Quantitative support for phylosymbiosis is provided by statistical methods evaluating higher microbiome variation between host species than within host species, topological similarities between the host phylogeny and microbiome dendrogram, and a positive association between host genetic relationships and microbiome beta diversity. Significant degrees of phylosymbiosis are prevalent, but not universal, in microbiomes of plants and animals from terrestrial and aquatic habitats. Consistent with natural selection shaping phylosymbiosis, microbiome transplant experiments demonstrate reduced host performance and/or fitness upon host-microbiome mismatches. Hybridization can also disrupt phylosymbiotic microbiomes and cause hybrid pathologies. The pervasiveness of phylosymbiosis carries several important implications for advancing knowledge of eco-evolutionary processes that impact host-microbiome interactions and future applications of precision microbiology. Important future steps will be to examine phylosymbiosis beyond bacterial communities, apply evolutionary modelling for an increasingly sophisticated understanding of phylosymbiosis, and unravel the host and microbial mechanisms that contribute to the pattern. This review serves as a gateway to experimental, conceptual and quantitative themes of phylosymbiosis and outlines opportunities ripe for investigation from a diversity of disciplines.

Phylosymbiosis is defined as microbial community relationships that recapitulate the phylogeny of hosts. As evidence for phylosymbiosis rapidly accumulates in different vertebrate and invertebrate holobionts, a central question is what evolutionary forces cause this pattern. We use intra- and interspecific gut microbiota transplants to test for evidence of selective pressures that contribute to phylosymbiosis. We leverage three closely related species of the parasitoid wasp model Nasonia that recently diverged between 0.4 and 1 million years ago: N. vitripennis , N. giraulti , and N. longicornis Upon exposure of germfree larvae to heat-inactivated microbiota from intra- or interspecific larvae, we measure larval growth, pupation rate, and adult reproductive capacity. We report three key findings: (i) larval growth significantly slows when hosts receive an interspecific versus intraspecific gut microbiota, (ii) marked decreases in pupation and resulting adult survival occur from interspecific gut microbiota exposure, and (iii) adult reproductive capacities including male fertility and longevity are unaffected by early life exposure to an interspecific microbiota. Overall, these findings reveal developmental and survival costs to Nasonia upon larval exposures to interspecific microbiota and provide evidence that selective pressures on phenotypes produced by host-microbiota interactions may underpin phylosymbiosis. IMPORTANCE Phylosymbiosis is an ecoevolutionary hypothesis and emerging pattern in animal-microbiota studies whereby the host phylogenetic relationships parallel the community relationships of the host-associated microbiota. A central prediction of phylosymbiosis is that closely related hosts exhibit a lower microbiota beta diversity than distantly related hosts. While phylosymbiosis has emerged as a widespread trend in a field often challenged to find trends across systems, two critical and understudied questions are whether or not phylosymbiosis is consequential to host biology and if adaptive evolutionary forces underpin the pattern. Here, using germfree rearing in the phylosymbiosis model Nasonia , we demonstrate that early life exposure to heat-inactivated microbiota from more distantly related species poses more severe developmental and survival costs than microbiota from closely related or the same species. This study advances a functional understanding of the consequences and potential selective pressures underpinning phylosymbiosis., (Copyright © 2019 van Opstal and Bordenstein.)

Skin is the largest organ of the body and represents the primary physical barrier between mammals and their external environment, yet the factors that govern skin microbial community composition among mammals are poorly understood. The objective of this research was to generate a skin microbiota baseline for members of the class Mammalia, testing the effects of host species, geographic location, body region, and biological sex. Skin from the back, torso, and inner thighs of 177 nonhuman mammals was sampled, representing individuals from 38 species and 10 mammalian orders. Animals were sampled from farms, zoos, households, and the wild. The DNA extracts from all skin swabs were amplified by PCR and sequenced, targeting the V3-V4 regions of bacterial and archaeal 16S rRNA genes. Previously published skin microbiome data from 20 human participants, sampled and sequenced using an identical protocol to the nonhuman mammals, were included to make this a comprehensive analysis. Human skin microbial communities were distinct and significantly less diverse than all other sampled mammalian orders. The factor most strongly associated with microbial community data for all samples was whether the host was a human. Within nonhuman samples, host taxonomic order was the most significant factor influencing skin microbiota, followed by the geographic location of the habitat. By comparing the congruence between host phylogeny and microbial community dendrograms, we observed that Artiodactyla (even-toed ungulates) and Perissodactyla (odd-toed ungulates) had significant congruence, providing evidence of phylosymbiosis between skin microbial communities and their hosts., Competing Interests: The authors declare no conflict of interest., (Copyright © 2018 the Author(s). Published by PNAS.)

Gut microbial communities provide many physiological functions to their hosts, especially in herbivorous animals. We still lack an understanding of how these microbial communities are structured across hosts in nature, especially within a given host species. Studies on laboratory mice have demonstrated that host genetics can influence microbial community structure, but that diet can overwhelm these genetic effects. We aimed to test these ideas in a natural system, the American pika (Ochotona princeps). First, pikas are high-elevation specialists with significant population structure across various mountain ranges in the USA, allowing us to investigate whether similarities in microbial communities match host genetic differences. Additionally, pikas are herbivorous, with some populations exhibiting remarkable dietary plasticity and consuming high levels of moss, which is exceptionally high in fibre and low in protein. This allows us to investigate adaptations to an herbivorous diet, as well as to the especially challenging diet of moss. Here, we inventoried the microbial communities of pika caecal pellets from various populations using 16S rRNA sequencing to investigate structuring of microbial communities across various populations with different natural diets. Microbial communities varied significantly across populations, and differences in microbial community structure were congruent with genetic differences in host population structure, a pattern known as "phylosymbiosis." Several microbial members (Ruminococcus, Prevotella, Oxalobacter and Coprococcus) were detected across all samples, and thus likely represent a "core microbiome." These genera are known to perform a number of services for herbivorous hosts such as fibre fermentation and the degradation of plant defensive compounds, and thus are likely important for herbivory in pikas. Moreover, pikas that feed on moss harboured microbial communities highly enriched in Melainabacteria. This uncultivable candidate phylum has been proposed to ferment fibre for herbivores, and thus may contribute to the ability of some pika populations to consume high amounts of moss. These findings demonstrate that both host genetics and diet can influence the microbial communities of the American pika. These animals may be novel sources of fibre-degrading microbes. Last, we discuss the implications of population-specific microbial communities for conservation efforts in this species., (© 2017 The Authors. Journal of Animal Ecology © 2017 British Ecological Society.)

Many female squids and cuttlefishes have a symbiotic reproductive organ called the accessory nidamental gland (ANG) that hosts a bacterial consortium involved with egg defense against pathogens and fouling organisms. While the ANG is found in multiple cephalopod families, little is known about the global microbial diversity of these ANG bacterial symbionts. We used 16S rRNA gene community analysis to characterize the ANG microbiome from different cephalopod species and assess the relationship between host and symbiont phylogenies. The ANG microbiome of 11 species of cephalopods from four families (superorder: Decapodiformes) that span seven geographic locations was characterized. Bacteria of class Alphaproteobacteria, Gammaproteobacteria, and Flavobacteriia were found in all species, yet analysis of amplicon sequence variants by multiple distance metrics revealed a significant difference between ANG microbiomes of cephalopod families (weighted/unweighted UniFrac, Bray-Curtis, P = 0.001). Despite being collected from widely disparate geographic locations, members of the family Sepiolidae (bobtail squid) shared many bacterial taxa including (~50%) Opitutae (Verrucomicrobia) and Ruegeria (Alphaproteobacteria) species. Furthermore, we tested for phylosymbiosis and found a positive correlation between host phylogenetic distance and bacterial community dissimilarity (Mantel test r = 0.7). These data suggest that closely related sepiolids select for distinct symbionts from similar bacterial taxa. Overall, the ANGs of different cephalopod species harbor distinct microbiomes and thus offer a diverse symbiont community to explore antimicrobial activity and other functional roles in host fitness.IMPORTANCEMany aquatic organisms recruit microbial symbionts from the environment that provide a variety of functions, including defense from pathogens. Some female cephalopods (squids, bobtail squids, and cuttlefish) have a reproductive organ called the accessory nidamental gland (ANG) that contains a bacterial consortium that protects eggs from pathogens. Despite the wide distribution of these cephalopods, whether they share similar microbiomes is unknown. Here, we studied the microbial diversity of the ANG in 11 species of cephalopods distributed over a broad geographic range and representing 15-120 million years of host divergence. The ANG microbiomes shared some bacterial taxa, but each cephalopod species had unique symbiotic members. Additionally, analysis of host-symbiont phylogenies suggests that the evolutionary histories of the partners have been important in shaping the ANG microbiome. This study advances our knowledge of cephalopod-bacteria relationships and provides a foundation to explore defensive symbionts in other systems.

Animals have a deep evolutionary relationship with microbial symbionts, such that individual microbes or an entire microbial community can diverge alongside the host. Here, we explore these host-microbe relationships in Echinometra, a sea urchin genus that speciated with the Isthmus of Panama and throughout the Indo-West Pacific. We find that the eggs from five Echinometra species generally associate with a species-specific bacterial community and that the relatedness of these communities is largely congruent with host phylogeny. Microbiome divergence per million years was higher in more recent speciation events than in older ones. We, however, did not find any bacterial groups that displayed co-phylogeny with Echinometra. Together, these findings suggest that the evolutionary relationship between Echinometra and their microbiota operates at the community level. We find no evidence suggesting that the associated microbiota is the evolutionary driver of Echinometra speciation. Instead, divergence between Echinometra and their microbiota is likely the byproduct of ecological, geographic, and reproductive isolations. [ABSTRACT FROM AUTHOR]

This article explores the evolutionary patterns and processes in animal microbiomes, specifically focusing on the correlation between microbiome composition and host phylogeny, the co-diversification of gut microbes with their hosts, and the mechanisms that shape microbiome variation within species. The findings provide a foundation for further research on the evolution of microbiomes and their impact on animal health. Additionally, the article discusses the consequences of animal-microbiome symbioses for the fitness of both hosts and symbionts, including the role of ecological drift and social transmission in shaping microbiome composition, the impact of diet-acquired microbiota on immune responses, and the ability of microbiomes to help hosts acclimate to environmental stressors. The article concludes by emphasizing the need for more research on the evolutionary patterns and processes of animal-microbiome symbioses. [Extracted from the article]

The symbiosis between a host and its microbiome is essential for host fitness, and this association is a consequence of the host's physiology and habitat. Sinocyclocheilus , the largest cavefish diversification of the world, an emerging multi-species model system for evolutionary novelty, provides an excellent opportunity for examining correlates of host evolutionary history, habitat, and gut-microbial community diversity. From the diversification-scale patterns of habitat occupation, major phylogenetic clades (A–D), geographic distribution, and knowledge from captive-maintained Sinocyclocheilus populations, we hypothesize habitat to be the major determinant of microbiome diversity, with phylogeny playing a lesser role. For this, we subject environmental water samples and fecal samples (representative of gut-microbiome) from 24 Sinocyclocheilus species, both from the wild and after being in captivity for 6 months, to bacterial 16S rRNA gene profiling using Illumina sequencing. We see significant differences in the gut microbiota structure of Sinocyclocheilus , reflective of the three habitat types; gut microbiomes too, were influenced by host-related factors. There is no significant association between the gut microbiomes and host phylogeny. However, there is some microbiome related structure at the clade level, with the most geographically distant clades (A and D) being the most distinct, and the two overlapping clades (B and C) showing similarities. Microbes inhabiting water were not a cause for significant differences in fish-gut microbiota, but water quality parameters were. Transferring from wild to captivity, the fish microbiomes changed significantly and became homogenized, signifying plastic changes and highlighting the importance of environmental factors (habitat) in microbiome community assembly. The core microbiome of this group, at higher taxonomic scale, resembled that of other teleost fishes. Our results suggest that divergent natural environments giving rise to evolutionary novelties underlying host adaptations, also includes the microbiome of these fishes. [ABSTRACT FROM AUTHOR]

Phylosymbiosis was recently formulated to support a hypothesis-driven framework for the characterization of a new, cross-system trend in host-associated microbiomes. Defining phylosymbiosis as 'microbial community relationships that recapitulate the phylogeny of their host', we review the relevant literature and data in the last decade, emphasizing frequently used methods and regular patterns observed in analyses. Quantitative support for phylosymbiosis is provided by statistical methods evaluating higher microbiome variation between host species than within host species, topological similarities between the host phylogeny and microbiome dendrogram, and a positive association between host genetic relationships and microbiome beta diversity. Significant degrees of phylosymbiosis are prevalent, but not universal, in microbiomes of plants and animals from terrestrial and aquatic habitats. Consistent with natural selection shaping phylosymbiosis, microbiome transplant experiments demonstrate reduced host performance and/or fitness upon host–microbiome mismatches. Hybridization can also disrupt phylosymbiotic microbiomes and cause hybrid pathologies. The pervasiveness of phylosymbiosis carries several important implications for advancing knowledge of eco-evolutionary processes that impact host–microbiome interactions and future applications of precision microbiology. Important future steps will be to examine phylosymbiosis beyond bacterial communities, apply evolutionary modelling for an increasingly sophisticated understanding of phylosymbiosis, and unravel the host and microbial mechanisms that contribute to the pattern. This review serves as a gateway to experimental, conceptual and quantitative themes of phylosymbiosis and outlines opportunities ripe for investigation from a diversity of disciplines. [ABSTRACT FROM AUTHOR]

Recently, our knowledge of the composition and complexity of tick microbial communities has increased and supports microbial impact on tick biology. Results support a phylogenetic association between ticks and their microbiota across evolution; this is known as phylosymbiosis. Herein, using published datasets, we confirm the existence of phylosymbiosis between Ixodes ticks and their microbial communities. The strong phylosymbiotic signal and the phylogenetic structure of microbial communities associated with Ixodid ticks revealed that phylosymbiosis may be a widespread phenomenon in tick–microbiota evolution. This finding supports the existence of a species-specific tick hologenome with a largely unexplored influence on tick biology and pathogen transmission. These results may provide potential targets for the construction of paratransgenic ticks to control tick infestations and tick-borne diseases. Microbes and ticks form a functional unity known as the tick hologenome. Coevolutionary events between ticks and symbionts have benefited tick fitness and adaptation. Phylosymbiosis occurs in ticks across their phylogeny. Phylosymbiosis between microbial communities and the tick genome provides the basis for future research on the role of microbes on tick biology and speciation. A better understanding of tick phylosymbiosis and hologenome, together with tick–microbiota and pathogen–microbiota interactions, would help in identifying the best targets for paratransgenesis in ticks for the control of tick-borne pathogens. [ABSTRACT FROM AUTHOR]