An official website of the United States government
Habitat specialization underpins biological processes from species distributions to speciation. However, organisms are often described as specialists or generalists based on a single niche axis, despite facing complex, multidimensional environments. Here, we analysed 236 environmental soil microbiomes across the United States and demonstrate that 90% of >1,200 prokaryotes followed one of two trajectories: specialization on all niche axes (multidimensional specialization) or generalization on all axes (multidimensional generalization). We then documented that this pervasive multidimensional specialization/generalization had many ecological and evolutionary consequences. First, multidimensional specialization and generalization are highly conserved with very few transitions between these two trajectories. Second, multidimensional generalists dominated communities because they were 73 times more abundant than specialists. Lastly, multidimensional specialists played important roles in community structure with ~220% more connections in microbiome networks. These results indicate that multidimensional generalization and specialization are evolutionarily stable with multidimensional generalists supporting larger populations and multidimensional specialists playing important roles within communities, probably stemming from their overrepresentation among pollutant detoxifiers and nutrient cyclers. Taken together, we demonstrate that the vast majority of soil prokaryotes are restricted to one of two multidimensional niche trajectories, multidimensional specialization or multidimensional generalization, which then has far-reaching consequences for evolutionary transitions, microbial dominance and community roles.
more »
« less
Host Specialisation, Immune Cross-Reaction and the Composition of Communities of Co-circulating Borrelia Strains
Abstract We use mathematical modelling to examine how microbial strain communities are structured by the host specialisation traits and antigenic relationships of their members. The model is quite general and broadly applicable, but we focus onBorrelia burgdorferi, the Lyme disease bacterium, transmitted by ticks to mice and birds. In this system, host specialisation driven by the evasion of innate immunity has been linked to multiple niche polymorphism, while antigenic differentiation driven by the evasion of adaptive immunity has been linked to negative frequency dependence. Our model is composed of two host species, one vector, and multiple co-circulating pathogen strains that vary in their host specificity and their antigenic distances from one another. We explore the conditions required to maintain pathogen diversity. We show that the combination of host specificity and antigenic differentiation creates an intricate niche structure. Unequivocal rules that relate the stability of a strain community directly to the trait composition of its members are elusive. However, broad patterns are evident. When antigenic differentiation is weak, stable communities are typically composed entirely of generalists that can exploit either host species equally well. As antigenic differentiation increases, more diverse stable communities emerge, typically around trait compositions of generalists, generalists and very similar specialists, and specialists roughly balanced between the two host species.
more »
« less
- Award ID(s):
- 1755370
- PAR ID:
- 10225702
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- Bulletin of Mathematical Biology
- Volume:
- 83
- Issue:
- 6
- ISSN:
- 0092-8240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Predicting pathogen emergence and spillover risk requires understanding the determinants of a pathogens' host range and the traits involved in host competence. While host competence is often considered a fixed species-specific trait, it may be variable if pathogens diversify across hosts. Balancing selection can lead to maintenance of pathogen polymorphisms (multiple-niche-polymorphism; MNP). The causative agent of Lyme disease, Borrelia burgdorferi ( Bb ), provides a model to study the evolution of host adaptation, as some Bb strains defined by their outer surface protein C ( ospC ) genotype, are widespread in white-footed mice and others are associated with non-rodent vertebrates (e.g. birds). To identify the mechanisms underlying potential strain × host adaptation, we infected American robins and white-footed mice, with three Bb strains of different ospC genotypes. Bb burdens varied by strain in a host-dependent fashion, and strain persistence in hosts largely corresponded to Bb survival at early infection stages and with transmission to larvae (i.e. fitness). Early survival phenotypes are associated with cell adhesion, complement evasion and/or inflammatory and antibody-mediated removal of Bb, suggesting directional selective pressure for host adaptation and the potential role of MNP in maintaining OspC diversity. Our findings will guide future investigations to inform eco-evolutionary models of host adaptation for microparasites.more » « less
-
Abstract The gut is continuously invaded by diverse bacteria from the diet and the environment, yet microbiome composition is relatively stable over time for host species ranging from mammals to insects, suggesting host-specific factors may selectively maintain key species of bacteria. To investigate host specificity, we used gnotobiotic Drosophila , microbial pulse-chase protocols, and microscopy to investigate the stability of different strains of bacteria in the fly gut. We show that a host-constructed physical niche in the foregut selectively binds bacteria with strain-level specificity, stabilizing their colonization. Primary colonizers saturate the niche and exclude secondary colonizers of the same strain, but initial colonization by Lactobacillus species physically remodels the niche through production of a glycan-rich secretion to favor secondary colonization by unrelated commensals in the Acetobacter genus. Our results provide a mechanistic framework for understanding the establishment and stability of a multi-species intestinal microbiome.more » « less
-
ABSTRACT Flowering plants can be visited by a wide diversity of pollinating insects; however, the structure of plant–insect interactions for non‐bee pollinators is not well‐known, even though non‐bee insects can play a central role in the pollination of many plant species. Pollination by non‐syrphid flies, such as bee flies (Bombylius majorL., Bombyliidae, Diptera), has often been underappreciated. Bee flies represent a diverse group of long‐tongue nectar‐feeding insects that are often reported as generalists who visit flowers indiscriminately. Here, we used individual‐based pollen transport networks to assess patterns of individual foraging in bee flies over two flowering seasons in a diverse co‐flowering community. Using this approach, we uncover the structure (e.g., modular vs. nested) of bee fly individual foraging and the degree of individual specialisation. We further evaluate the role of resource availability (floral abundance) and intraspecific trait variation (proboscis length and body size) in shaping individual specialisation. Overall, bee flies visited 20 different plant species. However, network analysis shows that individuals are more specialised and tend to partition the floral resource as reflected by the high degree of network modularity. Most bee fly individuals concentrate their foraging on only a few floral resources (two to four plant species) suggesting strong niche partitioning in this group of pollinators. This modular foraging pattern was not explained by differences in resource availability over the season. Proboscis length, however, was negatively related to the level of individual specialisation. Individuals with larger proboscis had larger foraging niches (less specialisation) perhaps due to easier access to a wide range of plant species with different floral tube sizes. Overall, our study reveals high individual specialisation and niche partitioning in bee‐fly interactions, mediated by differences in proboscis length, and with important implications for pollen transfer dynamics, plant–plant competition and plant reproductive success in diverse co‐flowering communities.more » « less
-
ABSTRACT Apex predators are typically considered dietary generalists, which often masks individual variability. However, individual specialization—consistent differences among individuals in resource use or ecological role—is common in apex predators. In some species, only a few specialized individuals can significantly impact prey populations. Leopard seals (Hydrurga leptonyx) are apex predators important to the structure and function of the Southern Ocean ecosystem. Though broadly described as generalists, little is known about their trophic ecology at the population or individual level. We analyzed δ13C and δ15N profiles in whiskers (n = 46) from 34 leopard seals in the Western Antarctic Peninsula to assess trophic variation. We also evaluated individual consistency across years using repeat samples from 7 seals over 2–10 years. We compared population and individual isotopic niche space and explored drivers of intraspecific variation in leopard seal trophic ecology. We find that leopard seals have a broad trophic niche (range: 6.96%–15.21‰) and are generalists at the population level. However, most individuals are specialists (59% for δ15N and δ13C), with only a few generalists (13% for δ15N, 6% for δ13C). Individuals also specialize at different trophic levels. Most variation in trophic ecology is driven by individual specialization, but sex and mass also contribute. We also find that some seals specialize over time, consistently foraging at the same trophic level, while others switch within and between years. This suggests some seals may disproportionately impact prey, especially when specialists consistently target specific species. Long‐term specialization by a few leopard seals likely contributed to the decline of the local Antarctic fur seal population. Our findings show the importance of examining individual specialization in leopard seals across their range to understand their impact on other prey populations. This approach should be applied to other apex predator populations, as a few specialists can significantly impact ecosystems.more » « less
