Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species
High dispersal rates are known to homogenize host’s population genetic structure in panmictic species and to disrupt host local adaptation to the environment. Long-distance dispersal might also spread micro-organisms across large geographical areas. However, so far, to which extent selection mechani...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-02-01
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| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00035/full |
| _version_ | 1818777256977235968 |
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| author | Mark Alan Frank Gillingham Arnaud Béchet Frank Cézilly Kerstin Wilhelm Manuel Rendón-Martos Fabrizio Borghesi Sergio Nissardi Nicola Baccetti Hichem Azafzaf Sebastian Menke Yves Kayser Simone Sommer |
| author_facet | Mark Alan Frank Gillingham Arnaud Béchet Frank Cézilly Kerstin Wilhelm Manuel Rendón-Martos Fabrizio Borghesi Sergio Nissardi Nicola Baccetti Hichem Azafzaf Sebastian Menke Yves Kayser Simone Sommer |
| author_sort | Mark Alan Frank Gillingham |
| collection | DOAJ |
| description | High dispersal rates are known to homogenize host’s population genetic structure in panmictic species and to disrupt host local adaptation to the environment. Long-distance dispersal might also spread micro-organisms across large geographical areas. However, so far, to which extent selection mechanisms that shape host’s population genetics are mirrored in the population structure of the enteric microbiome remains unclear. High dispersal rates and horizontal parental transfer may homogenize bacterial communities between breeding sites (homogeneous hypothesis). Alternatively, strong selection from the local environment may differentiate bacterial communities between breeding sites (heterogeneous hypothesis). Furthermore, selection from age-specific environmental or physiological factors may differentiate the microbiome between juveniles and adults. Here, we analyzed the cloacal bacterial 16S rRNA gene of fledgling greater flamingos, Phoenicopterus roseus, across nine western Mediterranean breeding sites and four breeding seasons (n = 731) and adult birds (n = 27) from a single site. We found that fledgling cloacal microbiome, as measured by alpha diversity, beta diversity, the relative abundance of assigned sequence variants (ASVs) belonging to a phylum and genus composition within phylum, varied significantly between sampling sites and across time within site despite high adult dispersal rates. The spatio-temporal effects were stronger on individual ASV absence/presence than on ASV abundance (i.e., than on core microbiome composition). Spatial effects had a stronger effect than temporal effects, particularly on ASV abundance. Our study supports the heterogeneous hypothesis whereby local environmental conditions select and differentiate bacterial communities, thus countering the homogenizing effects of high-dispersing host species. In addition, differences in core microbiome between adult vs. fledgling samples suggests that differences in age-specific environmental and/or physiological factors result in differential selection pressure of core enteric microbiome between age classes, even within the same environment. In particular, the genus Corynebacterium, associated with both seasonal fat uptake and migration in previous studies, was much more abundant in high-dispersing fledglings than in more resident adults. To conclude, selection mechanisms that shape the host’s genetic structure cannot be extended to the genetic structure of the enteric microbiome, which has important implications regarding our understanding of both host local adaptation mechanisms and enteric microbiome population genetics. |
| first_indexed | 2024-12-18T11:25:57Z |
| format | Article |
| id | doaj.art-ec1f810a8c65468da5972d648ad2d6a6 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-18T11:25:57Z |
| publishDate | 2019-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-ec1f810a8c65468da5972d648ad2d6a62022-12-21T21:09:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-02-011010.3389/fmicb.2019.00035420007Offspring Microbiomes Differ Across Breeding Sites in a Panmictic SpeciesMark Alan Frank Gillingham0Arnaud Béchet1Frank Cézilly2Kerstin Wilhelm3Manuel Rendón-Martos4Fabrizio Borghesi5Sergio Nissardi6Nicola Baccetti7Hichem Azafzaf8Sebastian Menke9Yves Kayser10Simone Sommer11Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, GermanyInstitut de Recherche de la Tour du Valat, Arles, FranceUniversité de Bourgogne, Equipe Ecologie Evolutive, UMR CNRS 6282 Biogéosciences, Dijon, FranceInstitute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, GermanyConsejería de Medio Ambiente y Ordenación del Territorio, R.N. Laguna de Fuente de Piedra, Fuente de Piedra, SpainDepartment of Biological Sciences, Geological and Environmental, University of Bologna, Ravenna, ItalyAnthus, s.n.c., Cagliari, ItalyIstituto Superiore per la Protezione e Ricerca Ambientale, Rome, ItalyAssociation “Les Amis des Oiseaux” (AAO/BirdLife Tunisie), Ariana Center, Ariana, TunisiaInstitute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, GermanyInstitut de Recherche de la Tour du Valat, Arles, FranceInstitute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, GermanyHigh dispersal rates are known to homogenize host’s population genetic structure in panmictic species and to disrupt host local adaptation to the environment. Long-distance dispersal might also spread micro-organisms across large geographical areas. However, so far, to which extent selection mechanisms that shape host’s population genetics are mirrored in the population structure of the enteric microbiome remains unclear. High dispersal rates and horizontal parental transfer may homogenize bacterial communities between breeding sites (homogeneous hypothesis). Alternatively, strong selection from the local environment may differentiate bacterial communities between breeding sites (heterogeneous hypothesis). Furthermore, selection from age-specific environmental or physiological factors may differentiate the microbiome between juveniles and adults. Here, we analyzed the cloacal bacterial 16S rRNA gene of fledgling greater flamingos, Phoenicopterus roseus, across nine western Mediterranean breeding sites and four breeding seasons (n = 731) and adult birds (n = 27) from a single site. We found that fledgling cloacal microbiome, as measured by alpha diversity, beta diversity, the relative abundance of assigned sequence variants (ASVs) belonging to a phylum and genus composition within phylum, varied significantly between sampling sites and across time within site despite high adult dispersal rates. The spatio-temporal effects were stronger on individual ASV absence/presence than on ASV abundance (i.e., than on core microbiome composition). Spatial effects had a stronger effect than temporal effects, particularly on ASV abundance. Our study supports the heterogeneous hypothesis whereby local environmental conditions select and differentiate bacterial communities, thus countering the homogenizing effects of high-dispersing host species. In addition, differences in core microbiome between adult vs. fledgling samples suggests that differences in age-specific environmental and/or physiological factors result in differential selection pressure of core enteric microbiome between age classes, even within the same environment. In particular, the genus Corynebacterium, associated with both seasonal fat uptake and migration in previous studies, was much more abundant in high-dispersing fledglings than in more resident adults. To conclude, selection mechanisms that shape the host’s genetic structure cannot be extended to the genetic structure of the enteric microbiome, which has important implications regarding our understanding of both host local adaptation mechanisms and enteric microbiome population genetics.https://www.frontiersin.org/article/10.3389/fmicb.2019.00035/fullgut microbiomedispersalpopulation differentiationgreater flamingosPhoenicopterus roseus |
| spellingShingle | Mark Alan Frank Gillingham Arnaud Béchet Frank Cézilly Kerstin Wilhelm Manuel Rendón-Martos Fabrizio Borghesi Sergio Nissardi Nicola Baccetti Hichem Azafzaf Sebastian Menke Yves Kayser Simone Sommer Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species Frontiers in Microbiology gut microbiome dispersal population differentiation greater flamingos Phoenicopterus roseus |
| title | Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species |
| title_full | Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species |
| title_fullStr | Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species |
| title_full_unstemmed | Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species |
| title_short | Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species |
| title_sort | offspring microbiomes differ across breeding sites in a panmictic species |
| topic | gut microbiome dispersal population differentiation greater flamingos Phoenicopterus roseus |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00035/full |
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