Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont.
Specialized host-microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeron...
Saved in:
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2024-04-01
|
| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3002304 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1841555644434350080 |
|---|---|
| author | Jason Z Chen Zeeyong Kwong Nicole M Gerardo Nic M Vega |
| author_facet | Jason Z Chen Zeeyong Kwong Nicole M Gerardo Nic M Vega |
| author_sort | Jason Z Chen |
| collection | DOAJ |
| description | Specialized host-microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host-microbe symbioses and microbe-microbe interactions within host-associated microbiomes. |
| format | Article |
| id | doaj-art-f0f73fe1437b43f7a5e661a43fad5bb7 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2024-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-f0f73fe1437b43f7a5e661a43fad5bb72025-01-08T05:30:25ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852024-04-01224e300230410.1371/journal.pbio.3002304Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont.Jason Z ChenZeeyong KwongNicole M GerardoNic M VegaSpecialized host-microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host-microbe symbioses and microbe-microbe interactions within host-associated microbiomes.https://doi.org/10.1371/journal.pbio.3002304 |
| spellingShingle | Jason Z Chen Zeeyong Kwong Nicole M Gerardo Nic M Vega Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. PLoS Biology |
| title | Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. |
| title_full | Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. |
| title_fullStr | Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. |
| title_full_unstemmed | Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. |
| title_short | Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont. |
| title_sort | ecological drift during colonization drives within host and between host heterogeneity in an animal associated symbiont |
| url | https://doi.org/10.1371/journal.pbio.3002304 |
| work_keys_str_mv | AT jasonzchen ecologicaldriftduringcolonizationdriveswithinhostandbetweenhostheterogeneityinananimalassociatedsymbiont AT zeeyongkwong ecologicaldriftduringcolonizationdriveswithinhostandbetweenhostheterogeneityinananimalassociatedsymbiont AT nicolemgerardo ecologicaldriftduringcolonizationdriveswithinhostandbetweenhostheterogeneityinananimalassociatedsymbiont AT nicmvega ecologicaldriftduringcolonizationdriveswithinhostandbetweenhostheterogeneityinananimalassociatedsymbiont |