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Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation.

Barelli C, Albanese D, Donati C, Pindo M, Dallago C, Rovero F, Cavalieri D, Tuohy KM, Hauffe HC, De Filippo C - Sci Rep (2015)

Bottom Line: While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest.Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics.Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

View Article: PubMed Central - PubMed

Affiliation: Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy.

ABSTRACT
The expansion of agriculture is shrinking pristine forest areas worldwide, jeopardizing the persistence of their wild inhabitants. The Udzungwa red colobus monkey (Procolobus gordonorum) is among the most threatened primate species in Africa. Primarily arboreal and highly sensitive to hunting and habitat destruction, they provide a critical model to understanding whether anthropogenic disturbance impacts gut microbiota diversity. We sampled seven social groups inhabiting two forests (disturbed vs. undisturbed) in the Udzungwa Mountains of Tanzania. While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest. Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics. Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

No MeSH data available.


Related in: MedlinePlus

Microbiota profile distances as a function of physical distances.Pairwise unweighted UniFrac distances stratified by within social groups, and between sympatric and allopatric groups. P < 10−9 (Wilcoxon rank sum test, Bonferroni corrected) for all comparisons (a). Unweighted UniFrac distance plotted against geographical distances between GPS points of sample sites (b). The straight line is the linear least squares regression to the data.
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f7: Microbiota profile distances as a function of physical distances.Pairwise unweighted UniFrac distances stratified by within social groups, and between sympatric and allopatric groups. P < 10−9 (Wilcoxon rank sum test, Bonferroni corrected) for all comparisons (a). Unweighted UniFrac distance plotted against geographical distances between GPS points of sample sites (b). The straight line is the linear least squares regression to the data.

Mentions: In order to disentangle whether gut microbiota diversity is due to environmental or heritable factors we compare family social groups from sympatric (i.e. co-occurring in the same forest geographical location) and allopatric (i.e. geographically separated forest) host populations. Although geographical variation is often also confounded by variation in host genetic background, the population analysis of our study groups (using a set of 10 microsatellite loci) showed that gene flow between the two forests ceased recently (small but significant FST). Therefore, only minor genetic differences between the colobus living in the Ma and Mw forests are expected (Ruiz-Lopez et al., personal communication). Figure 7a shows that the median of the unweighted UniFrac distance between samples within the same social group is significantly smaller (P < 10−9, Wilkoxon rank sum test, Bonferroni correction) than that between individuals of sympatric groups (co-occurring in the same forest), which is in turn significantly smaller than the mean distance between individuals of allopatric groups (inhabiting different forests). Plausible explanations of this pattern include vertical transmission between parents and offspring, or horizontal transmission between group members that share the same home range and are in close contact with each other while feeding or allogrooming41. Similarly, in rural Papua New Guineans low variation (beta-diversity) among individuals was explained through environmental sharing and dispersal limitation42. However, we did not found significant differences between sympatric social groups within forests (Supplementary Fig. S5).


Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation.

Barelli C, Albanese D, Donati C, Pindo M, Dallago C, Rovero F, Cavalieri D, Tuohy KM, Hauffe HC, De Filippo C - Sci Rep (2015)

Microbiota profile distances as a function of physical distances.Pairwise unweighted UniFrac distances stratified by within social groups, and between sympatric and allopatric groups. P < 10−9 (Wilcoxon rank sum test, Bonferroni corrected) for all comparisons (a). Unweighted UniFrac distance plotted against geographical distances between GPS points of sample sites (b). The straight line is the linear least squares regression to the data.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4595646&req=5

f7: Microbiota profile distances as a function of physical distances.Pairwise unweighted UniFrac distances stratified by within social groups, and between sympatric and allopatric groups. P < 10−9 (Wilcoxon rank sum test, Bonferroni corrected) for all comparisons (a). Unweighted UniFrac distance plotted against geographical distances between GPS points of sample sites (b). The straight line is the linear least squares regression to the data.
Mentions: In order to disentangle whether gut microbiota diversity is due to environmental or heritable factors we compare family social groups from sympatric (i.e. co-occurring in the same forest geographical location) and allopatric (i.e. geographically separated forest) host populations. Although geographical variation is often also confounded by variation in host genetic background, the population analysis of our study groups (using a set of 10 microsatellite loci) showed that gene flow between the two forests ceased recently (small but significant FST). Therefore, only minor genetic differences between the colobus living in the Ma and Mw forests are expected (Ruiz-Lopez et al., personal communication). Figure 7a shows that the median of the unweighted UniFrac distance between samples within the same social group is significantly smaller (P < 10−9, Wilkoxon rank sum test, Bonferroni correction) than that between individuals of sympatric groups (co-occurring in the same forest), which is in turn significantly smaller than the mean distance between individuals of allopatric groups (inhabiting different forests). Plausible explanations of this pattern include vertical transmission between parents and offspring, or horizontal transmission between group members that share the same home range and are in close contact with each other while feeding or allogrooming41. Similarly, in rural Papua New Guineans low variation (beta-diversity) among individuals was explained through environmental sharing and dispersal limitation42. However, we did not found significant differences between sympatric social groups within forests (Supplementary Fig. S5).

Bottom Line: While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest.Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics.Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

View Article: PubMed Central - PubMed

Affiliation: Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy.

ABSTRACT
The expansion of agriculture is shrinking pristine forest areas worldwide, jeopardizing the persistence of their wild inhabitants. The Udzungwa red colobus monkey (Procolobus gordonorum) is among the most threatened primate species in Africa. Primarily arboreal and highly sensitive to hunting and habitat destruction, they provide a critical model to understanding whether anthropogenic disturbance impacts gut microbiota diversity. We sampled seven social groups inhabiting two forests (disturbed vs. undisturbed) in the Udzungwa Mountains of Tanzania. While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest. Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics. Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

No MeSH data available.


Related in: MedlinePlus