Biogeography of the ecosystems of the healthy human body

Background

Characterizing the biogeography of the microbiome of healthy humans is essential for understanding microbial associated diseases. Previous studies mainly focused on a single body habitat from a limited set of subjects. Here, we analyzed one of the largest microbiome datasets to date and generated a biogeographical map that annotates the biodiversity, spatial relationships, and temporal stability of 22 habitats from 279 healthy humans.

Results

We identified 929 genera from more than 24 million 16S rRNA gene sequences of 22 habitats, and we provide a baseline of inter-subject variation for healthy adults. The oral habitat has the most stable microbiota with the highest alpha diversity, while the skin and vaginal microbiota are less stable and show lower alpha diversity. The level of biodiversity in one habitat is independent of the biodiversity of other habitats in the same individual. The abundances of a given genus at a body site in which it dominates do not correlate with the abundances at body sites where it is not dominant. Additionally, we observed the human microbiota exhibit both cosmopolitan and endemic features. Finally, comparing datasets of different projects revealed a project-based clustering pattern, emphasizing the significance of standardization of metagenomic studies.

Conclusions

The data presented here extend the definition of the human microbiome by providing a more complete and accurate picture of human microbiome biogeography, addressing questions best answered by a large dataset of subjects and body sites that are deeply sampled by sequencing.     

Biogeography and history of the Mediterranean bird fauna

With 366 species of breeding birds, the Mediterranean region is a "hot spot" of species diversity. Many biogeographic realms contributed to the establishment of the extant fauna, which makes this region a crossroads for birds, but the two most important realms are the large forest blocks that extend today over Eurasia and the semi-arid belts of the southern and southwestern Palaearctic. The few groups that presumably differentiated within the Mediterranean basin are mostly birds of open habitats and shrublands (e.g. Sylvia spp.), whereas few species evolved in Mediterranean forests dominated by sclerophyllous evergreen tree species. We suggest this results from the history of vegetation belts and their associated faunas during the Pleistocene. On the whole, in contrast to other groups of vertebrates, the bird fauna is fairly homogeneously distributed all over the basin although there are some regional-specific trends in species assemblages, mostly on the basis of habitat selection and biogeographic origin. Many species of eastern and southeastern origin invaded the Mediterranean basin on the northern side of the sea up to the Balkan peninsula and the southern side to the Atlantic coast. The extant biogeographic patterns of the Mediterranean bird fauna are interpreted in the light of the Quaternary history shared by the biotas of the western Palaearctic in relation to the cycle of climatic changes which produced periodic huge spatiotemporal migrations of communities and populations. The severe human impact that started c. 8000-10,000 years ago resulted not so much in species extinctions as in dramatic changes in distributional patterns, complicating the reconstruction of biogeographic scenarios.     

Facilitation of Quercus ilex recruitment by shrubs in Mediterranean open woodlands

Question: Insufficient tree regeneration threatens the long‐term persistence of biodiverse Mediterranean open oak woodlands. Could shrubs, scarce due to decades of management (clearing and ploughing), facilitate holm oak recruitment at both acorn and seedling stages? Location: Open oak woodlands in Central Spain. Methods: Plots with four acorns were planted: (1) under the canopy of the spiny shrub Genista hirsuta, (2) in a small cage, protecting against ungulates, (3) in a shaded cage, protecting against ungulates and sun, and (4) in open grassland. Sets of these four treatments were spatially grouped according to a randomised block design, with 16 blocks near (< 10 m) and 16 away from (> 20 m) parent trees to test for distance‐related survival. Plots were regularly checked for seed removal. After emergence one seedling per plot (97 in total) was selected and its survival monitored. Results: Three months after sowing, 199 of 512 acorns were removed, predominantly by rodents. Acorn removal occurred at each treatment but was highest under shrubs. Eight months after sowing, seedling survival was highest under shrubs (50%), followed by shaded cages (16%), open grassland (4%) and cages (0%). Main mortality cause was drought (90%), killing most seedlings between June and July. No seedlings died from ungulate browsing. Conclusion: Shrubs demonstrated clear net facilitative effects for Quercus ilex recruitment, despite higher seed removal. Shading appears the crucial factor facilitating seedling survival. We therefore propose that lack of shrubs contributes largely to tree recruitment failure in Mediterranean open woodlands; management should aim at conserving shrubs.     

The efficiency of nitrogen retranslocation from leaf biomass in Quercus ilex ecosystems

Nitrogen retranslocation from senescing leaves represents a crucial adaptation by tree species towards a more efficient use of this nutrient. As a result, this part of the nitrogen cycle has received increasing attention in recent years. However, there remain strong discrepancies with respect to the factors responsible for interspecific differences in the efficiency of this process.In the present work the seasonal pattern of leaf growth and the movement of nitrogen in leaves have been studied in a series of Quercus ilex plots with different levels of rainfall and soil quality in central-western Spain, as well as in 20 other woody species typical of this area. The percentage of nitrogen retranslocated was estimated from the difference between the maximum mass of nitrogen stored in the leaf biomass and the amount of this nutrient returned annually to the soil through leaf fall. Q. ilex appears as one of the least efficient species in the Mediterranean region in the recovery of nitrogen from senescing leaves (29.7% of the maximum pool). Furthermore, the older leaves of Q. ilex do not show the cycles of nitrogen withdrawal during new flushes of shoot growth, such as occurs in Pinus spp. This suggests that older leaves in Q. ilex do not play an important role as nitrogen storage organs.     

Leaf physiological responses to extreme droughts in Mediterranean Quercus ilex forest

Global climate change is expected to result in more frequent and intense droughts in the Mediterranean region. To understand forest response to severe drought, we used a mobile rainfall shelter to examine the impact of spring and autumn rainfall exclusion on stomatal (S_L) and non‐stomatal (NS_L) limitations of photosynthesis in a Quercus ilex ecosystem. Spring rainfall exclusion, carried out during increasing atmospheric demand and leaf development, had a larger impact on photosynthesis than autumn exclusion, conducted at a time of mature foliage and decreasing vapour pressure deficit. The relative importance of NS_L increased with drought intensity. S_L and NS_L were equal once total limitation (T_L) reached 60%, but NS_L greatly exceeded S_L during severe drought, with 76% NS_L partitioned equally between mesophyll conductance (MC_L) and biochemical (B_L) limitations when T_L reached 100%. Rainfall exclusion altered the relationship between leaf water potential and photosynthesis. In response to severe mid‐summer drought stress, A_n and V_cmax were 75% and 72% lower in the spring exclusion plot than in the control plot at the same pre‐dawn leaf water potential. Our results revealed changes in the relationship between photosynthetic parameters and water stress that are not currently included in drought parameterizations for modelling applications.     

Plastic bimodal growth in a Mediterranean mixed-forest of Quercus ilex and Pinus halepensis

Mediterranean tree species have evolved to face seasonal water shortages, but may fail to cope with future increases in drought frequency and intensity. We investigated stem radial increment dynamics in two typical Mediterranean tree species, Aleppo pine (Pinus halepensis), a drought-avoiding species, and holm oak (Quercus ilex), a drought-tolerant species, in a mixed forest and on contrasting slope aspects (south- and north-facing). Intra- and inter-annual growth patterns were modelled using the VS-Lite2 model for each tree species and slope-aspect. Both species showed a bimodal growth pattern, with peaks coinciding with favourable conditions in spring and autumn. A bimodal growth pattern is always observed in P. halepensis, while in Q. ilex is facultative, which suggests different strategies adopted by these species to cope with summer drought. More specifically, trees on south-facing slope showed a more evident bimodal pattern and more intra-annual density fluctuations. In recent decades, the intensity of both growth peaks has diminished and drifted away due to the increased summer drought. The VS-Lite2 model reveals a niche partitioning between both species. Differences in growing season’s length and timings of growth peaks in both species are relevant for their coexistence and should be considered for estimating mixed-forest responses under climate change scenarios.     

Long-term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest

In the Mediterranean basin, precipitation is expected to decline as a consequence of climate change. The response of a Quercus ilex forest in southern France to such a decline in water availability was studied using a 4-year throughfall exclusion experiment. Seasonal courses of sap flow and leaf water potential were obtained from 2004 to 2007 and used to characterize tree water relations in a control and a dry treatment. The experiment reduced the average precipitation input to the soil by 29%, and resulted in a 23% reduction in annual transpiration. Soil water potential was significantly lower in the dry treatment only during summer drought, but transpiration was reduced all year round even during well-watered periods. Despite a tight stomatal control over transpiration, whole-tree hydraulic conductance was found to be lower in the trees growing in the driest conditions. This reduction in water transport capacity was observed jointly with a reduction in leaf transpiring area. Canopy leaf area decreased by 18% in the dry treatment as a consequence of the throughfall exclusion, which was found to validate the ecohydrological equilibrium theory.     

生物地理学理论的发展

生物地理学是一门占老而又年轻的学科,近几十年来又获得了新的发展。本文较详尽地介绍了该学科的基本思想和基本研究方法,并对生物地理学理论发展的历史和各种理论的基本论点及理论假说进行了重点讨论。此外,作者对该学科的发展提出了自己的思考。     

Macrofungal diversity and ecology in two Mediterranean forest ecosystems

The macrofungal species richness and community assemblages in Italian native woodlands of oaks and Carpinus betulus and non-native woodlands of Pinus spp., Cupressus sempervirens and Eucalyptus camaldulensis were examined through the collection of basidiomata and ascomata over 1 year. The sampling in Collestrada (Umbria) and Pizzo Manolfo (Sicily) forests revealed 216 species of macrofungi. The results indicate differences in macromycete richness and diversity patterns between the two sites. The dominant tree species of the two sites were different; thus, the Collestrada forests had higher mycorrhizal species richness, while the Pizzo Manolfo forest had a higher relative number of saprotroph macrofungi. The macrofungal community of Quercus frainetto woodland from Collestrada forest was richer and more diverse than the other site's woodland types. This study highlighted that both Collestrada and Pizzo Manolfo forests provide a habitat for diverse macrofungal species, not in the least ectomycorrhizal species.     

Large-Scale Patterns of Quercus ilex, Quercus suber, and Quercus pyrenaica Regeneration in Central-Western Spain

In Central-Western Spain, forests and woodlands composed of Quercus sp. support outstanding levels of biodiversity, but there is increasing concern about their long-term persistence due to a lack of regeneration. We hypothesize that this regenerative lack is operating on a large geographic scale; that there are differences in the abundance of regeneration between three oak species; that oak regeneration is governed mainly by forest management and structure; and that shrubs act as important physical protectors of seedlings and saplings. We analyzed whether densities of oak seedlings and saplings in several size classes were related to stand-structure, understory, and physiographic variables potentially affecting regeneration. Data collected at a regional level (1 km × 1 km grid) by the Spanish Forest Inventory were evaluated from 2,816 plots. Results revealed that regeneration failure was common for all size categories, from small seedlings to large saplings, and for the three oak species studied, especially the evergreens. Of the Quercus ilex, Q. suber, and Q. pyrenaica plots studied, 49%, 62%, and 20% were lacking any small seedlings, and 82%, 96%, and 56% did not have any large saplings, respectively. Regeneration was positively correlated with tree cover and density, especially of small and medium-sized trees, and negatively correlated with the presence of large trees, indicating that regeneration failure is mostly associated with more open, uniform, and/or aged woodlands. Regeneration densities of Q. ilex and Q. suber were positively correlated with all understory variables, suggesting that the presence of pioneer shrubs represent a major safe site for early tree recruitment, independent from specific shrub species.     

Comparative ecophysiological effects of drought on seedlings of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera and Quercus ilex

Ecophysiological and structural traits of seedlings of the water-saver Pinus halepensis and the water-spenders Quercus coccifera and Q. ilex were studied in response to water stress under greenhouse conditions. Water deficit reduced stomatal conductance (g _s) and, as a consequence, both net CO₂ assimilation (A) and transpiration rate (E) were also reduced. Water stress also emphasized midday down-regulation of the photochemical efficiency (dynamic photoinhibition) reducing quantum yield of noncyclic electron transport (Φ_PSII), photochemical quenching (qP) and photochemical efficiency of the open reaction centres of PSII () and involved an increase of thermal dissipation of excess energy. However, water stress not only induced dynamic photoinhibition but also brought a reduction in F _v/F _m (chronic photoinhibition). Despite the water-saving strategy of P. halepensis that limited net CO₂ assimilation, this species showed a higher photochemical efficiency and lower photoinhibition than Quercus species. This was not the result of a different photochemical quenching but was linked to a higher value of , indicating a less severe photo-inactivation of PSII. Water stress resulted in a loss of pigment content and in an increase of the carotenoids/chlorophyll ratio, antioxidant capacity and the biomass rate allocated to roots as opposed to that assigned to leaves. P. halepensis showed a lower photoinhibition and antioxidant activity than Quercus species due to its lower pigment content and higher proportion of carotenoids allowing P. halepensis to use, in a more effective way, the lesser excess energy absorbed.     

Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex

We analysed the ectomycorrhizal (ECM) fungal diversity in a Mediterranean old-growth Quercus ilex forest stand from Corsica (France), where Arbutus unedo was the only other ECM host. On a 6400 m2 stand, we investigated whether oak age and host species shaped below-ground ECM diversity. Ectomycorrhizas were collected under Q. ilex individuals of various ages (1 yr seedlings; 3-10 yr saplings; old trees) and A. unedo. They were typed by ITS-RFLP analysis and identified by match to RFLP patterns of fruitbodies, or by sequencing. A diversity of 140 taxa was found among 558 ectomycorrhizas, with many rare taxa. Cenococcum geophilum dominated (35% of ECMs), as well as Russulaceae, Cortinariaceae and Thelephoraceae. Fungal species richness was comparable above and below ground, but the two levels exhibited < 20% overlap in fungal species composition. Quercus ilex age did not strongly shape ECM diversity. The two ECM hosts, A. unedo and Q. ilex, tended to share few ECM species (< 15% of the ECM diversity). Implications for oak forest dynamics are discussed.     

Ancient and current gene flow between two distantly related Mediterranean oak species, Quercus suber and Q. ilex

Background and Aims

Quercus suber and Q. ilex are distantly related and their distributions partially overlap. They hybridize occasionally, but the complete replacement of Q. suber chloroplast DNA (cpDNA) by that of Q. ilex was identified in two specific geographical areas. The objective of this study was to determine whether the contrasting situation reflected current or recent geographical interspecies gene flow variation or was the result of ancient introgression.

Methods

cpDNA PCR-RFLPs (restriction fragment length polymorphisms) and variation at ten nuclear microsatellite loci were analysed in populations of each species, in 16 morphologically intermediate individuals and the progeny of several of them. Interspecies nuclear introgression was based on individual admixture rates using a Bayesian approach with no a priori species assignment, and on a maximum-likelihood (ML) method, using allele frequencies in the allopatric populations of each species as controls. Gene flow was compared specifically between populations located within and outside the specific areas.

Key Results

High interspecies nuclear genetic differentiation was observed, with twice the number of alleles in Q. ilex than in Q. suber. According to Bayesian assignment, approx. 1 % of individuals had a high probability of being F₁ hybrids, and bidirectional nuclear introgression affected approx. 4 % of individuals in each species. Hybrid and introgressed individuals were identified predominantly in mixed stands and may have a recent origin. Higher proportions including allospecific genes recovered from past hybridization were obtained using the ML method. Similar rates of hybridization and of nuclear introgression, partially independent of cpDNA interspecies transfer suggestive of gene filtering, were obtained in the populations located within and outside the areas of complete cpDNA replacement.

Conclusions

The results did not provide evidence for geographical variation in interspecies gene flow. In contrast, historical introgression is supported by palynological records and constitutes the more reliable origin of cpDNA replacement in specific regions.Key words: cpDNA PCR-RFLPs, nuclear microsatellite (nSSR) variation, hybridization, interspecies genetic introgression, Quercus suber, Quercus ilex     

Biogeography of limno-terrestrial Tardigrada, with particular reference to the Antarctic fauna

The Tardigrada is a cosmopolitan phylum of pre-Pangaean origin, yet tardigrade families and genera show distinct biogeographic components isolated by two major geological events. Separate Laurasian and Gondwanan familial clusters correlate with the Triassic disintegration of Pangaea, while discrete Antarctic, Australian and New Zealand familial/generic clusters relate to the subsequent Jurassic/Cretaceous disintegration of Gondwana.     

Transpiration and stomatal behaviour of Quercus ilex plants during the summer in a Mediterranean carbon dioxide spring

Variations in the water relations and stomatal response of Quercus ilex were analysed under field conditions by comparing trees at two locations in a Mediterranean environment during two consecutive summers (1993 and 1994). We used the heat-pulse velocity technique to estimate transpirational water use of trees during a 5 month period from June to November 1994. At the end of sap flow measurements, the trees were harvested, and the foliage and sapwood area measured. A distinct environmental gradient exists between the two sites with higher atmospheric CO₂ concentrations in the proximity of a natural CO₂ spring. Trees at the spring site have been growing for generations in elevated atmospheric CO₂ concentrations. At both sites, maximum leaf conductance was related to predawn shoot water potential. The effects of water deficits on water relations and whole-plant transpiration during the summer drought were severe. Leaf conductance and water potential recovered after major rainfall in September to predrought values. Sap flow, leaf conductance and predawn water potential decreased in parallel with increases in hydraulic resistance, reaching a minimum in mid-summer. These relationships are in agreement with the hypothesis of the stomatal control of transpiration to prevent desiccation damage but also to avoid ‘runaway embolism’. Trees at the CO₂ spring underwent less reduction in hydraulic resistance for a given value of predawn water potential. The decrease in leaf conductance caused by elevated CO₂ was limited and tended to be less at high than at low atmospheric vapour pressure deficit. Mean (and diurnal) sap flux were consistently higher in the control site trees than in the CO₂ spring trees. The degree of reduction in water use between the two sites varied among the summer periods. The control site trees had consistently higher sap flow at corresponding values of either sapwood cross-sectional area or foliage area. Larger trees displayed smaller differences than smaller trees, between the control and the CO₂ spring trees. A strong association between foliage area and sapwood cross-sectional area was found in both the control and the CO₂ spring trees, the latter supporting a smaller foliage area at the corresponding sapwood stem cross-sectional area. The specific leaf area (SLA) of the foliage was not influenced by site. The results are discussed in terms of the effects of elevated CO₂ on plant water use at the organ and whole-tree scale.