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Award Abstract # 1046149
Dimensions: The Microbial Basis of Animal Speciation

NSF Org: DEB
Division Of Environmental Biology
Recipient: VANDERBILT UNIVERSITY
Initial Amendment Date: September 23, 2010
Latest Amendment Date: June 2, 2014
Award Number: 1046149
Award Instrument: Continuing Grant
Program Manager: Simon Malcomber
smalcomb@nsf.gov
 (703)292-8227
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: March 1, 2011
End Date: February 28, 2017 (Estimated)
Total Intended Award Amount: $1,268,861.00
Total Awarded Amount to Date: $1,270,109.00
Funds Obligated to Date: FY 2010 = $689,965.00
FY 2013 = $293,642.00

FY 2014 = $286,502.00
History of Investigator:
  • Seth Bordenstein (Principal Investigator)
    seth.bordenstein@vanderbilt.edu
Recipient Sponsored Research Office: Vanderbilt University
110 21ST AVE S
NASHVILLE
TN  US  37203-2416
(615)322-2631
Sponsor Congressional District: 05
Primary Place of Performance: Vanderbilt University
110 21ST AVE S
NASHVILLE
TN  US  37203-2416
Primary Place of Performance
Congressional District:
05
Unique Entity Identifier (UEI): GTNBNWXJ12D5
Parent UEI:
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001011DB NSF RESEARCH & RELATED ACTIVIT
01001314DB NSF RESEARCH & RELATED ACTIVIT

01001415DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 7968, 9150, 9169, EGCH
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

One of the central questions in biodiversity research is how did Life go from one to currently 1.8 million described species? For most animals, species are categorized as groups of individuals that interbreed with each other. Therefore, new animal species can arise by genetic mutations that ultimately prevent two groups from producing hybrid offspring. However, animal species may also change by acquiring differences in the millions of bacteria that typically live in symbiotic relationships inside them. This research addresses a major gap in our knowledge about how biodiversity arises: whether or not the symbiotic community of bacteria within a host species can contribute to hybrid lethality between species. To that end, the investigation will address three aims using several species of the model insect Nasonia that vary in their level of hybrid lethality: (i) Test the prediction that bacterial diversity is species-specific and abnormally reduced in hybrids that die (ii) Test the prediction that immunity genes are preferentially misexpressed in hybrids, and associate specific gene expression differences to the alterations in the hybrids' bacterial community (iii) Test if hybrid mortality is due to either a reduction in beneficial bacteria or an increase in pathogenic bacteria. The studies will integrate genetic, taxonomic, and functional dimensions of animal-microbe symbioses to comprehensively determine the consequences of bacterial symbionts on speciation in a model system. Taxonomically, the investigators will characterize new species of bacteria and existing species of bacteria in novel functions. Preliminary studies suggest 25% of the bacterial species in Nasonia are new to science. Genetic aspects of the studies will include the effects that hybridization can have on animal gene expression and the genetic diversity of their bacterial symbionts. Functionally, this work will unravel the host's dependence on bacterial symbionts throughout development, and test whether bacterial symbionts are as important as genes in the generation of new, animal species.
Broader impacts of this project include (i) the development of a new undergraduate course at Vanderbilt University that will involve students in the research, (ii) the creation of an online repository for taxonomic information on the symbionts discovered in this research, (iii) dissemination of data through publically accessible databases, and (iv) extensions to understanding speciation and symbiosis in new ways across all animals, including humans. Finally, the proposed research will provide training to one graduate student, one research assistant, and several undergraduates involved in volunteerships, internships, and research for credit.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 25)
A. Saulsberry, M. Pinchas, A. Noll, J.A. Lynch, S.R. Bordenstein, R.M. Brucker "Establishment of F1 hybrid mortality in real time" BMC Evolutionary Biology , v.17 , 2017 DOI: 10.1186/s12862-017-0879-1
A.W. Brooks, K.D. Kohl, R.M. Brucker, E.J. van Opstal, S.R. Bordenstein "Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History" PLOS Biology , 2016 https://doi.org/10.1371/journal.pbio.2000225
Bordenstein, S.R. and K.R. Theis "Host biology in light of the microbiome: Ten principles of holobionts and hologenomes" PLOS Biology , v.13 , 2015 , p.e1002226 10.1371/journal.pbio.1002226
Brucker, R.B. and S.R. Bordenstein "In vitro cultivation of the Hymenoptera genetic model, Nasonia" PLOS One , v.7 , 2012 , p.e51269 10.1371/journal.pone.0051269
Brucker, R.M. and S.R. Bordenstein "Speciation by Symbiosis" Trends in Ecology and Evolution , v.27 , 2012 , p.443
Brucker, R.M. and S.R. Bordenstein "The capacious hologenome" Zoology , v.115 , 2013 , p.260 DOI http://dx.doi.org/10.1016/j.zool.2013.08.003
Brucker, R.M. and S.R. Bordenstein "The hologenomic basis of speciation: Gut bacteria cause hybrid mortality in the genus Nasonia" Science , 2013 , p.DOI: 10.1
Brucker, R.M., L.J. Funkhouser, S. Setia, R. Pauly and S.R. Bordenstein "Insect innate immunity database (IIID): An annotation tool for identifying immune genes in insect genomes" PLOS One , v.7 , 2012 , p.e45125 10.1371/journal.pone.0045125
B.W. Richmond, R.M. Brucker, W. Han, R-H Du, Y. Zhang, D-S Cheng, L. Gleaves, R. Abdolrasulnia, D. Polosukhina, P.E. Clark, S.R. Bordenstein, T.S. Blackwell, V.V. Polosukhin "Airway bacteria drive a progressive COPD-like phenotype in mice with polymeric immunoglobulin receptor deficiency" Nature Communications , v.7 , 2016 doi:10.1038/ncomms11240
D.P. Bojanova and S.R. Bordenstein "Fecal Transplants: What Is Being Transferred?" PLOS Biology , v.14:7 , 2016 , p.e1002503 https://doi.org/10.1371/journal.pbio.1002503
Funkhouser-Jones, L.J., Martinez-Rodriguez P., Sehnert, S.*, Toribio-Fernandez R., Pita M., Bella J.L., and S.R. Bordenstein "Wolbachia co-infection in a hybrid zone: Discovery of horizontal gene transfers from two Wolbachia supergroups to an animal genome" PeerJ , v.3 , 2015 , p.e1479 https://doi.org/10.7717/peerj.1479
(Showing: 1 - 10 of 25)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The Microbial Basis of Speciation

One of the central questions of biodiversity research is how did Life go from one to currently millions of species today? Despite the centrality of this question, an appreciation of the role that bacterial infections play in assisting one host species to split into two and so on remains in its early stages. Our work focuses on a particular group of closely-related animal species that notably split into four species less than a million years ago. The animals are tiny green and gold wasps called Nasonia.  

Because Nasonia are a group of young species, males and females can still breed with each other to varying degrees. Depending upon the species used, the hybrids either live or die at a high rate during development of the larvae. This natural variation in hybrid survival between the Nasonia species affords an opportunity to study what makes some hybrids die while others live in the same group of related species. Therefore, we set out to test the unique hypothesis that bacteria in the intestinal tracts of Nasonia contribute to why hybrids die between species.

We uncovered four key results. First, each Nasonia species harbors a distinguishable gut bacterial community that is specific to their developmental stage and gender. Second, each community is uniquely qualified to affect host functions of their resident host species, namely the timing of development and survival to adulthood. Third, hybridization between the Nasonia species leads to an altered gut bacterial community in hybrids that eventually die, but not in hybrids that live. This altered gut microbial community is associated with increased immune gene esxpression in hybrids. Fourth, elimination of the gut bacterial community in hybrids rescues their survivability. Finally, transplanting a gut bacterial community into these bacteria-free hybrids causes the hybrid death once again.

These results show, for the first time, that hybrid death can be dependent upon the presence of a gut bacterial community. In other words, the resident and helpful bacterial community within one animal species can go awry in hybrids that have a deficient immune response and cause hybrid death. Charles Darwin and the 20th-century pioneers of biology may have been astonished to see the countless roles that bacteria play in animal evolution, including the origin of species.

Broader Impacts

This project trained at least five graduate students and ten undergraduates in hands-on biological research. Five undergraduates notably earned authorship on scientific publications. This work continued to bridge the fields of microbial symbiosis and speciation, and it produced the first germ-free rearing protocol for the Nasonia model system. In addition, this project developed the Insect Innate Immune Database that serves as a free online portal of annotated immune genes for model insects used in biological research. Several symbiosis internet sites were created around this work as well including FaceBook community pages, the Symbionticism Blog and a YouTube video channel.  The Vanderbilt Microbiome Initiative, a transinstitutional community of microbiome investigators, emerged because of the training and expertise developed from this proposal. Sustained outreach efforts to Metro Nashville Public High Schools now exist in which students use biodiversity and molecular biology tools to discover bacterial symbionts in local insects. Finally, emerging research initiatives are now conceptualizing an individual animal or plant as a holobiont - the sum of a host and its associated microbes that can vary in time, space and function to affect phenotype and fitness.

 

 


Last Modified: 05/30/2017
Modified by: Seth R Bordenstein

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