Disentangling the Coevolutionary Histories of Animal Gut Microbiomes

Animals associate with microbes in complex interactions with profound fitness consequences. These interactions play an enormous role in the evolution of both partners, and recent advances in sequencing technology have allowed for unprecedented insight into the diversity and distribution of these ass...

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Main Author: Sanders, Jon G.
Other Authors: Pierce, Naomi E., Girguis, Peter R., Knoll, Andrew H., Alm, Eric
Format: Thesis
Language:English
Published: 2015
Subjects:
Online Access:http://nrs.harvard.edu/urn-3:HUL.InstRepos:17463127
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spelling ftharvardudash:oai:dash.harvard.edu:1/17463127 2023-05-15T15:37:00+02:00 Disentangling the Coevolutionary Histories of Animal Gut Microbiomes Sanders, Jon G. Pierce, Naomi E. Girguis, Peter R. Knoll, Andrew H. Alm, Eric 2015-05 application/pdf http://nrs.harvard.edu/urn-3:HUL.InstRepos:17463127 en eng Sanders, Jon G. 2015. Disentangling the Coevolutionary Histories of Animal Gut Microbiomes. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences. http://nrs.harvard.edu/urn-3:HUL.InstRepos:17463127 Biology General Microbiology Ecology Thesis or Dissertation text 2015 ftharvardudash 2022-04-05T18:35:00Z Animals associate with microbes in complex interactions with profound fitness consequences. These interactions play an enormous role in the evolution of both partners, and recent advances in sequencing technology have allowed for unprecedented insight into the diversity and distribution of these associations. However, our understanding of the processes generating those patterns remains in its infancy. Here, I explore variation in microbiomes across two animal lineages—ants and mammals—to tease apart the role of these process in the evolution of gut microbiota. First, I explore patterns of phylogenetic correlation in gut microbiota of herbivorous Cephalotes ants and hominid apes. By examining the sensitivity of phylogenetic correlation to analytical parameters, I show that these outwardly similar patterns are likely to be the result of very different processes in each host lineage. Next, I examine in more depth the interacting effects of diet and phylogeny on the structure of baleen whale microbiomes. Whales consume a diet that differs dramatically from that of their closest extant relatives, the herbivorous artiodactyls. I use a combination of marker gene and shotgun metagenomic sequencing to show that a phylogentically conserved host trait, the multichambered gut, leads to functional and taxonomic similarities of whale gut microbiomes to those of their herbivorous ancestors via the fermentation of animal polysaccharides in the exoskeletons of their prey. Finally, I return to ants to examine how major shifts in the nature of gut microbial association correspond to host ecology. Using measures of absolute bacterial abundance, rather than diversity, I test the hypothesis that evolution of symbiosis with microbes has facilitated ants’ dominance of tropical rainforest canopies. Surprisingly, I find differences in the abundance of gut bacteria in different ant lineages that span many orders of magnitude, suggesting that evolutionary transitions in the functional role of symbiosis in this animal lineage correspond not only to changes in the diversity of these associations, but to changes in kind. The results of these studies help to clarify the roles of history and selection in structuring animal gut microbiota, hinting that the interaction of these factors may fundamentally differ between animal lineages. Biology, Organismic and Evolutionary Microbiome; coevolution Thesis baleen whale Harvard University: DASH - Digital Access to Scholarship at Harvard
institution Open Polar
collection Harvard University: DASH - Digital Access to Scholarship at Harvard
op_collection_id ftharvardudash
language English
topic Biology
General
Microbiology
Ecology
spellingShingle Biology
General
Microbiology
Ecology
Sanders, Jon G.
Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
topic_facet Biology
General
Microbiology
Ecology
description Animals associate with microbes in complex interactions with profound fitness consequences. These interactions play an enormous role in the evolution of both partners, and recent advances in sequencing technology have allowed for unprecedented insight into the diversity and distribution of these associations. However, our understanding of the processes generating those patterns remains in its infancy. Here, I explore variation in microbiomes across two animal lineages—ants and mammals—to tease apart the role of these process in the evolution of gut microbiota. First, I explore patterns of phylogenetic correlation in gut microbiota of herbivorous Cephalotes ants and hominid apes. By examining the sensitivity of phylogenetic correlation to analytical parameters, I show that these outwardly similar patterns are likely to be the result of very different processes in each host lineage. Next, I examine in more depth the interacting effects of diet and phylogeny on the structure of baleen whale microbiomes. Whales consume a diet that differs dramatically from that of their closest extant relatives, the herbivorous artiodactyls. I use a combination of marker gene and shotgun metagenomic sequencing to show that a phylogentically conserved host trait, the multichambered gut, leads to functional and taxonomic similarities of whale gut microbiomes to those of their herbivorous ancestors via the fermentation of animal polysaccharides in the exoskeletons of their prey. Finally, I return to ants to examine how major shifts in the nature of gut microbial association correspond to host ecology. Using measures of absolute bacterial abundance, rather than diversity, I test the hypothesis that evolution of symbiosis with microbes has facilitated ants’ dominance of tropical rainforest canopies. Surprisingly, I find differences in the abundance of gut bacteria in different ant lineages that span many orders of magnitude, suggesting that evolutionary transitions in the functional role of symbiosis in this animal lineage correspond not only to changes in the diversity of these associations, but to changes in kind. The results of these studies help to clarify the roles of history and selection in structuring animal gut microbiota, hinting that the interaction of these factors may fundamentally differ between animal lineages. Biology, Organismic and Evolutionary Microbiome; coevolution
author2 Pierce, Naomi E.
Girguis, Peter R.
Knoll, Andrew H.
Alm, Eric
format Thesis
author Sanders, Jon G.
author_facet Sanders, Jon G.
author_sort Sanders, Jon G.
title Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
title_short Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
title_full Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
title_fullStr Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
title_full_unstemmed Disentangling the Coevolutionary Histories of Animal Gut Microbiomes
title_sort disentangling the coevolutionary histories of animal gut microbiomes
publishDate 2015
url http://nrs.harvard.edu/urn-3:HUL.InstRepos:17463127
genre baleen whale
genre_facet baleen whale
op_relation Sanders, Jon G. 2015. Disentangling the Coevolutionary Histories of Animal Gut Microbiomes. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences.
http://nrs.harvard.edu/urn-3:HUL.InstRepos:17463127
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