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Research Spending & Results

Award Detail

Awardee:UNIVERSITY OF MONTANA
Doing Business As Name:University of Montana
PD/PI:
  • Douglas J Emlen
  • (406) 243-2535
  • doug.emlen@mso.umt.edu
Award Date:08/28/2009
Estimated Total Award Amount: $ 654,452
Funds Obligated to Date: $ 660,452
  • FY 2012=$126,691
  • FY 2010=$250,523
  • FY 2009=$145,138
  • FY 2013=$138,100
Start Date:08/15/2009
End Date:07/31/2015
Transaction Type:Grant
Agency:NSF
Awarding Agency Code:4900
Funding Agency Code:4900
CFDA Number:47.074
Primary Program Source:040100 NSF RESEARCH & RELATED ACTIVIT
Award Title or Description:Collaborative Research: Genetic mechanisms of conditional-expression and trait exaggeration in weapons of sexual selection
Federal Award ID Number:0919781
DUNS ID:010379790
Parent DUNS ID:079602596
Program:Integrtv Ecological Physiology

Awardee Location

Street:32 CAMPUS DRIVE
City:Missoula
State:MT
ZIP:59812-0001
County:Missoula
Country:US
Awardee Cong. District:00

Primary Place of Performance

Organization Name:University of Montana
Street:32 CAMPUS DRIVE
City:Missoula
State:MT
ZIP:59812-0001
County:Missoula
Country:US
Cong. District:00

Abstract at Time of Award

Animals produce a bewildering diversity of ornaments and weapons that function in male contests over reproductive access to females. Two characteristics are common in the most elaborate of these structures: disproportionate growth yielding exaggerated trait sizes, and growth that is more sensitive to nutrition than is the growth of other, non-sexually-selected, structures (e.g. antlers in moose or elk reach extreme sizes in the largest bulls, and antler growth is especially sensitive to the nutritional state of the animal). Despite intense interest in the evolution of these sexually selected traits, almost nothing is known of the genes or the developmental mechanisms responsible for disproportionate/ exaggerated growth, or of the mechanisms linking nutrition with the amount of trait growth. This proposal addresses a fundamental gap in understanding the evolutionary potential of ornaments and weapons of sexual selection: What are the genes and developmental/ physiological processes that underlie nutrition-dependent expression and exaggerated growth? The premise for this project is that to understand the evolution of these structures requires exploration of the details of how they develop. The long-term goal is to understand how physiology and development interact with the environment to generate diversity in morphological and behavioral phenotypes. The objectives are to identify genes and associated physiological pathways responsible for generating exaggerated weapon growth, and nutrition-dependent phenotypic plasticity. The investigators will (1) test whether the mechanisms generating nutrition-dependent expression are the same as those generating exaggerated growth, and (2) compare these mechanisms for two weapons (horns & mandibles) in three lineages of beetle representing three independent origins of enlarged male weapons (dung beetles, rhinoceros beetles, & stag beetles). The integrative approach utilized will shed light on physiological and developmental pathways involved with nutrition-dependent phenotypic plasticity in animals generally, and will provide one of the most comprehensive studies to date linking variation in male condition with the expression of sexually selected traits - a central tenet of current theories of sexual selection. A core objective is the cross-training of young scientists in genetics, development, physiology and evolution. The postdoc and students involved with this project will spend extensive periods in all three labs actively learning techniques and interacting and collaborating with all three PIs. The PIs are committed to training undergraduates in all aspects of the research process, and will incorporate innovative teaching methods in science that embrace diversity; the very nature of this system lends itself to learner-centered investigations. The focal species are a fantastic resource for outreach activities and the PIs will use these animals in educational programs designed to enhance STEM learning in K-12 students as well as in informal science education environments, including visiting local school classrooms in both WA and MT, supporting the WSU insect museum, and aiding with a new Montana insect zoo.

Publications Produced as a Result of this Research

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Tien Van Truong; Byun, Doyoung; Lavine, Laura Corley; Emlen, Douglas J.; Park, Hoon Cheol; Kim, Min Jun "Flight behavior of the rhinoceros beetle Trypoxylus dichotomus during electrical nerve stimulation" BIOINSPIRATION & BIOMIMETICS, v.7, 2012, p.036021. doi:10.1088/1748-3182/7/3/036021 

McCullough, E. Emlen, D. "Evaluating the costs of a sexually selected weapon: big horns at a small price." Animal Behaviour, v.86, 2013, p.977.

Gotoh, H. Cornette, R. Koshikawa, S. Okada, Y. Corley-Lavine, L. Emlen, D. Miura, T. "Juvenile Hormone Regulates Extreme Mandible Growth in Male Stag Beetles" PLoS One, v.6, 2011, p.e21139.

Corley-Lavine, L. Hahn, L. Garczynski, S. Warren, I. Dworkin, I. Emlen, D. "Cloning and characterization of a mRNA encoding an insulin receptor from the horned scarab beetle Onthophagus nigriventris (Coleoptera: Scarabaeidae)." Archives of Insect Biochemistry and Physiology, v.82, 2012, p.43.

Gotoh, H., Miyakawa, H., Ishikawa, A., Ishikawa, Y., Sugime, Y., Corley Lavine, L., Emlen, D.J. and T. Miura. "Developmental link between sex and nutrition: doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles." PloS Genetics (with cover), v., 2014, p.. doi:10.1371/journal.pgen.1004098 

Gotoh, Hiroki; Cornette, Richard; Koshikawa, Shigeyuki; Okada, Yasukazu; Lavine, Laura Corley; Emlen, Douglas J.; Miura, Toru "Juvenile Hormone Regulates Extreme Mandible Growth in Male Stag Beetles" PLOS ONE, v.6, 2011, p.e21139. doi:10.1371/journal.pone.0021139 

McCullough, E. Ledger, K. J. O'Brien, D. M. Emlen, D. J. "Variation in the allometry of exaggerated rhinoceros beetle horns." Animal Behaviour, v.109, 2015, p.133.

Van Truong, T. Byun, D. Corley-Lavine, L. Emlen, D. Park, H. C. Kim, M. J. "Flight behavior of the rhinoceros beetle Trypoxylus dichotomus during electrical nerve stimulation" Bioinspiration & Biomimetics, v.7, 2012, p.036021.

Gotoh, H. Miyakawa, H. Ishikawa, A. Ishikawa, Y. Sugime, Y. Emlen, D. J. Lavine, L. C. Miura, T. "Developmental link between sex and nutrition: doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles" PLoS Genetics, v.10, 2014, p..

Warren, I. Gotoh, H. Dworkin, I. Emlen, D. Corley-Lavine, L. "A general mechanism for conditional expression of exaggerated sexually- selected traits" BioEssays, v.35, 2013, p.889.

Johns, A., Gotoh, H., McCullough, E., Emlen, D., and Corley-Lavine, L. "Heightened condition-dependent growth of sexually selected weapons in the rhinoceros beetle, Trypoxylus dichotomus (Coleoptera: Scarabaeidae)." Integrative and Comparative Biology, v., 2014, p.. doi:10.1093/icb/icu041 

Corley Lavine, L., Hahn, LL, Garczynski, SF, Warren, IA, Dworkin, IM and DJ Emlen "Cloning and characterization of an insulin receptor gene from the horned scarab beetle Onthophagus nigriventris (Coleoptera: Scarabaeidae)" Archives of Insect Biochemistry & Physiology, v.82, 2012, p.43-57. doi:10.1002/arch.21072 

Gotoh, Hiroki, Cornette, Richard, Koshikawa, Shigeyuki, Okada, Yasukazu, Corley Lavine, Laura, Emlen, Douglas, Miura, Toru "Juvenile hormone regulates extreme mandible growth in male stag beetles" PloS One, v., 2011, p..

Lavine, L., Gotoh, H., Brent, C. S., Dworkin, I. and Emlen, D. "Exaggerated trait growth in insects" Annual Review of Entomology, v.60, 2015, p.453. doi:10.1146/annurev-ento-010814-021045 

McCullough, Erin L.; Weingarden, Paul R.; Emlen, Douglas J. "Costs of elaborate weapons in a rhinoceros beetle: how difficult is it to fly with a big horn?" Behavioral Ecology, v.23, 2012, p.1042-1048. doi:10.1093/beheco/ars069 

McCullough, E. Weingarden, P. Emlen, D. J. "Costs of elaborate weapons in a rhinoceros beetle: how difficult is it to fly with a big horn?" Behavioral Ecology, v., 2012, p.. doi:10.1093/beheco/ars069 

Ian A Warren, J. Cristobal Vera, Annika Johns, Robert A Zinna, James H Marden, Doug J Emlen, Ian Dworkin and Laura C Lavine. "Insights into the development and evolution of exaggerated traits using de novo transcriptomes of two species of horned scarab beetles." PLoS One, v.9, 2013, p.e88364.

Hattori, A. Miyakawa, H., Ishikawa, Y., Miyazaki, S., Okada, Y., Cornette, R., Corley Lavine, L., Emlen, D.J., Koshikawa, S., and T. Miura. "Soldier morphogenesis in the damp-wood termite is regulated by the insulin signaling pathway." Journal of Experimental Zoology Part B Molecular & Developmental Evolution., v.in pres, 2013, p.295.

McCullough, E., Tobalske, B., Emlen, D. "Structural adaptations to diverse fighting styles in sexually selected weapons." Proceedings of the National Academy of Sciences, v., 2014, p.. doi:10.1073/pnas.1409585111 

Emlen DJ, Warren I, Johns A, Dworkin I, Corley Lavine L. "A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons." Science, v.337, 2012, p.860-864. doi:10.1126/science.1224286 

McCullough, E., Emlen, D. "Evaluating the costs of a sexually selected weapon: big horns at a small price." Animal Behaviour, v.86, 2013, p.977.

Emlen, D. Warren, I. Johns, A. Dworking, I. Corley-Lavine, L. "A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons." Science, v.337, 2012, p.860.

Warren IA, Gotoh H, Dworkin IM, Emlen DJ, Lavine LC. "A general mechanism for conditional expression of sexually-selected traits." BioEssays, v.35, 2013, p.889.

Warren, I. A. Vera, J. C. Zinna, R. Marden, J. Emlen, D. Dworking, I. Lavine, L. "Insights into the development and evolution of exaggerated traits using de novo transcriptomes of two species of horned scarab beetles." PLoS One, v.9, 2013, p.e88364.

Gotoh, H. Hust, J. A. Miura, T. Niimi, T. Emlen, D. J. Lavine, L. C. "The Fat/Hippo Signaling pathway links within-disc morphogen patterning to whole-animal signals during phenotypically plastic growth." Developmental Dynamics, v.244, 2015, p.1039.

Johns, A. Gotoh, H. McCullough, E. Emlen, D. J. Lavine, L. C. "Heightened condition-dependent growth of sexually selected weapons in the rhinoceros beetle, Trypoxylus dichotomus (Coleoptera: Scarabaeidae)" Integrative and Comparative Biology, v., 2014, p.. doi:10.1093/icb/icu041 


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.

What generates the striking diversity in animal form in the animal kingdom? This is one of the most fundamental, unanswered questions in evolutionary biology. Our research project addressed this problem by focusing specifically on the exaggerated traits of animals. Many species of beetles exhibit remarkably large and ostentatious male-specific traits such as horns and enlarged jaws. These exaggerated male-specific traits are weapons that males use to fight over access to females and ultimately, to sire the most offspring.  We and others have found that males with the largest horns and mandibles win fights and have the most offspring. We have also found that the size of these male horns and mandibles is tightly linked to the amount of food they are able to consume when they are in the immature stage. Our goal in this project was to identify the genetic and physiological mechanisms that control the growth of beetle horns and mandibles during development under different nutritional conditions. We used the latest technologies to sequence the genes that are expressed during specific, critical periods during beetle development to identify these mechanisms in three different species of beetles. We chose these three species of beetles because, while they all have male-specific exaggerated traits, the type of trait (head horn versus thoracic horn versus enlarged mandibles) is different, and these weapons are considered to have evolved independently of each other. We also tested the function of genes that we identified to discover the role that these genes have in the development and growth of these traits. Our results are the first comprehensive survey of gene expression from three different beetle weapons that combine function with form. In addition, we have found that the physiological mechanisms and genes that are involved are not all the same. This was not what we expected, and it is very exciting for the evolution of sexually-selected traits in general. More importantly, we can now say that animal diversity in form is not controlled by single genes or pathways, but by complex interactions of genes and physiological signals, even between relatively closely related beetle species! These results are also exciting because we show that animals sensitive to the nutrition environment can use different pathways to sense these inputs; in essence, animals are not restricted to one pathway but are flexible in their response depending on their evolutionary history. Finally, our results have important implications for the generality of physiological and genetic interactions in animal communication and signaling in sexually-selected traits.

In addition to the scientific achievements that have resulted from our project, we are also very proud of our broader impacts. Specifically we have trained postdoctoral fellows and offered them professional development opportunities, we have mentored graduate students and undergraduate students in authentic research, we have disseminated the results of our work in peer-reviewed publications, invited reviews, and invited presentations around the world, and we have conducted outreach and engagement events to K-12 as well as the community in general. We have also been trained, and trained others in exciting new ways to engage women, minorities, and all students in science and science education.


Last Modified: 12/14/2015
Modified by: Douglas J Emlen

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