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Feminization of Male Brown Treesnake Methyl Ketone Expression via Steroid Hormone Manipulation

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Abstract

Pheromones are useful tools for the management of invasive invertebrates, but have proven less successful in field applications for invasive vertebrates. The brown treesnake, Boiga irregularis, is an invasive predator that has fundamentally altered the ecology of Guam. The development of control tools to manage Boiga remains ongoing. Skin-based, lipophilic pheromone components facilitate mating in brown treesnakes, with females producing the same long-chain, saturated and monounsaturated (ketomonoene) methyl ketones known to function as pheromones in garter snakes, Thamnophis sirtalis. Boiga also express novel, diunsaturated methyl ketones (ketodienes) with a purported function as a sex pheromone. In our study, we implanted 17 β-estradiol in adult male brown treesnakes in order to manipulate methyl ketone expression as sex attractants, an effect that would mirror findings with garter snakes. Specifically, estrogen promoted production of two ketomonoenes, pentatriaconten-2-one and hexatriaconten-2-one, and suppressed production of one ketodiene, heptatriacontadien-2-one. In bioassays, estrogen-implanted males elicited tongue-flicking and chin rubbing behavior from unmanipulated males, though the responses were weaker than those elicited by females. On Guam, wild males exhibited greatest responses to whole female skin lipid extracts and only weak responses to the methyl ketone fractions from females and implanted males. Our results suggest that sex identity in brown treesnakes may be conferred by the ratio of ketomonoenes (female) to ketodienes (male) from skin lipids and may be augmented by a sex-specific endocrine signal (estradiol). However, a blend of long-chain methyl ketones alone is not sufficient to elicit maximal reproductive behaviors in male Boiga.

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Acknowledgements

G. Gathright (U.S. Department of Agriculture [USDA], National Wildlife Research Center [NWRC]) conducted the implantation surgeries. J. Noll and S. Ashton-Cromwell assisted with fractionation of samples at James Madison University (JMU). The project was funded primarily by an agreement between the USDA NWRC and Washington and Lee University (WLU)(14-7483-1088-CA) and more recently by an agreement between USDA NWRC and JMU (16-7442-1225-CA), made possible by funding from the Department of Defense Joint Regions Marianas (N61128-14-MP-001AG). MRP and SMP were supported by funding from an HHMI institutional grant (WLU), and MRP also received a partial grant from the Lenfest Foundation of WLU and a faculty summer research supplement from the College of Science and Mathematics (JMU). GC/MS analysis was conducted at the Roy J. Carver Biotechnology Center at the University of Illinois, with significant assistance from A. Ulanov. Bioassays on Guam were made possible through field collections and animal care provided by C. Robinson and M. Viernes of the U.S. Geological Survey (USGS). A. Bristol, L. Moore, and A. Narzynski assisted with very late-night bioassays. All Guam work was initiated and coordinated by E. Holldorf and R. Reed (USGS), with special thanks to J. Savidge (Colorado State University). All procedures involving the use of vertebrate animals were approved by the IACUC of the USDA NWRC (QA-2339) and USGS (2016-10). The manuscript and figures were improved following helpful critiques by three anonymous reviewers.

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Correspondence to M. Rockwell Parker.

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Parker, M.R., Patel, S.M., Zachry, J.E. et al. Feminization of Male Brown Treesnake Methyl Ketone Expression via Steroid Hormone Manipulation. J Chem Ecol 44, 189–197 (2018). https://doi.org/10.1007/s10886-018-0935-3

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  • DOI: https://doi.org/10.1007/s10886-018-0935-3

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