Award Abstract # 1146410
Collaborative Research: Epigenetic, transcriptomic, and behavioral impacts of a maternal signal during wasp caste development

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: IOWA STATE UNIVERSITY OF SCIENCE AND TECHNOLOGY
Initial Amendment Date: January 17, 2012
Latest Amendment Date: March 20, 2014
Award Number: 1146410
Award Instrument: Continuing Grant
Program Manager: Michelle Elekonich
melekoni@nsf.gov
 (703)292-7202
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: April 1, 2012
End Date: March 31, 2016 (Estimated)
Total Intended Award Amount: $431,000.00
Total Awarded Amount to Date: $439,498.00
Funds Obligated to Date: FY 2012 = $150,000.00
FY 2013 = $164,498.00

FY 2014 = $125,000.00
History of Investigator:
  • Amy Toth (Principal Investigator)
    amytoth@iastate.edu
Recipient Sponsored Research Office: Iowa State University
1350 BEARDSHEAR HALL
AMES
IA  US  50011-2103
(515)294-5225
Sponsor Congressional District: 04
Primary Place of Performance: Iowa State University
IA  US  50011-2207
Primary Place of Performance
Congressional District:
Unique Entity Identifier (UEI): DQDBM7FGJPC5
Parent UEI: DQDBM7FGJPC5
NSF Program(s): Animal Behavior
Primary Program Source: 01001213DB NSF RESEARCH & RELATED ACTIVIT
01001314DB NSF RESEARCH & RELATED ACTIVIT

01001415DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1228, 7218, 9150, 9178, 9251
Program Element Code(s): 765900
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Many studies on humans and rodents have aimed at understanding how maternal care influences the behavior and health of offspring. Because it is hard to separate the effects of maternal behavior itself from effects of the environment, many fundamental questions remain unanswered: To what extent can maternal care itself directly affect the long-term behavior and physiology of offspring? Can maternal care completely or partially overcome environmental stressors? Does maternal care trigger genetic changes in offspring that mediate long-term effects?

Toth and Jeanne will use a new behavioral system to address these questions. Mother paper wasps (Polistes) feed and care for larvae throughout their development. In the process, maternal wasps physically vibrate their larvae by striking their antennae on nest cells. This behavior, which can be simulated using a piezoelectric device, has profound effects on offspring. Vibrated larvae become workers, whereas un-vibrated wasps become queens. This unique system can be used to experimentally dissect how maternal behavior affects offspring.

The researchers will use state-of-the art DNA sequencing methods to characterize what types of genetic changes (e.g. gene activation or chemical DNA modifications) are induced in offspring in response to the interactions of an environmental factor (nutritional stress) and a maternal behavior (vibrations).

This work will provide new information on the extent to which maternal behavior can affect the fate of offspring, how these effects may be modulated by stressors in the environment, and the genetic mechanisms underlying this process. The project will involve the training of a postdoctoral researcher, several undergraduates, and a high school teacher. The results will be disseminated to the scientific community and new insights shared at school and community outreach events.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Berens, A.J., Hunt, J.H., Toth, A.L. "Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects" Mol. Biol. Evol , v.32 , 2015 , p.690 10.1093/molbev/msu330
Berens, A.J., Hunt, J.H., Toth, A.L. "Nourishment level affects caste-related gene expression in Polistes wasps" BMC Genomics , v.16 , 2015 , p.235 10.1186/s12864-015-1410-y
Jandt, JM, Thomson, J, Geffre, AC, Toth, AL "Lab rearing environment perturbs social traits: a case study with Polistes wasps" Behavioral Ecology , v.26 , 2016 , p.1274-1284
Jandt, JM, Tibbetts, EA, Toth, AL. "Polistes paper wasps: a model genus for the study of social dominance hierarchies." Insectes Sociaux , v.61 , 2014 , p.11 10.1007/s00040-013-0328-0
Jandt, JM; Toth, AL "Chapter Three-Physiological and Genomic Mechanisms of Social Organization in Wasps (Family: Vespidae)" Advances in Insect Physiology , v.48 , 2015 , p.95-130
Sheehan, Michael J; Botero, Carlos A; Hendry, Tory A; Sedio, Brian E; Jandt, Jennifer M; Weiner, Susan; Toth, Amy L; Tibbetts, Elizabeth A; "Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps" Ecology letters , v.18 , 2015 , p.1057-1067
Standage, Daniel S; Berens, Ali J; Glastad, Karl M; Severin, Andrew J; Brendel, Volker P; Toth, Amy L; "Genome, transcriptome and methylome sequencing of a primitively eusocial wasp reveal a greatly reduced DNA methylation system in a social insect" Molecular Ecology , v.25 , 2016
Toth, Amy L; Sumner, Seirian; Jeanne, Robert L; "Patterns of longevity across a sociality gradient in vespid wasps" Current Opinion in Insect Science , v.16 , 2016 , p.28-35

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.

In this project, we aimed to gain a deeper understanding of the mechanisms by which mothers can shape the developmental fate of their offspring.  To do this, we used social paper wasps, Polistes fuscatus, excellent models for studying maternal and social behavior.  These wasps make small colonies initiated by founding queens, devoted mothers who spend weeks defending and feeding their offspring.  Interestingly, not all offspring are equal; those produced early in the season are all female and become workers, who are typically sterile, short-lived, and toil for the colony.  On the other hand, offspring produced later in the season are destined to reproduce rather than work—either as males, or as “gynes”— long-lived wasp princesses who will become the next generation of queens.

 

How do wasps produce such unequal daughters? We used the striking variation in P. fuscatus female developmental fate into different castes (workers or gynes) to study the role of maternal interactions in shaping offspring traits.  We found that there are thousands of genes showing different activity between developing workers and gynes, setting them up for possessing vastly different adult physiology and behavior. Further experiments revealed queen mom’s behavior toward her developing larvae has a profound effect in two important ways.  First, there is food.  Early season larvae are underfed by mom and typically become workers.  We found that restricted feeding alone can lead to the suppression of gyne-related genes, sending larvae on a developmental track to become workers.  Second, how mom interacts with larvae is also key.  Intriguingly, founding queens target vibrational signals at their larvae, called “antennal drumming”.  Previous work suggested these maternal signals lead daughters to become leaner, a worker-like trait.  We designed small “piezoelectric devices” that vibrate nests at mom’s frequency, and attached them to wasp nests in the field.  We found that these vibrations can also influence gene activity during development.  Some gyne-related genes are also shut down by vibrations, while others were influenced by the combination of low food and vibrations.  Thus, both nutritional and tactile maternal influences, and their interaction, work together to influence the caste fate of offspring.

 

These data provide new insights into how the maternal social environment can influence gene activity in developing offspring.  Importantly, these differences in gene activity have the potential to set up different life trajectories for offspring, leading to adults with vastly different physiology and behavior.  

 


Last Modified: 08/09/2016
Modified by: Amy Toth

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