Insight into the neuroendocrine basis of signal evolution: a case study in foot-flagging frogs
- 190 Downloads
A hallmark of sexual selection is the evolution of elaborate male sexual signals. Yet, how the physiology of an animal changes to support a new or modified signal is a question that has remained largely unanswered. Androgens are important in regulating male reproductive behavior, therefore, selection for particular signals may drive the evolution of increased androgenic sensitivity in the neuro-motor systems underlying their production. Studies of the neuroendocrine mechanisms of anuran sexual signaling provide evidence to support this idea. Here, we highlight two such cases: first, a large body of work in Xenopus frogs demonstrates that sexually dimorphic androgen receptor (AR) expression in the laryngeal nerves and muscles underlies sexually dimorphic vocal behavior, and second, our own work showing that the recent evolution of a hind limb signal (known as the “foot flag”) in Staurois parvus is accompanied by a dramatic increase in androgenic sensitivity of the thigh muscles that control limb movement. Together, these examples illustrate that the evolutionary modification or gain of a sexual signal is linked with a novel pattern of AR expression in the tissues that support it. We suggest that such co-evolution of AR expression and sex-specific or species-specific signaling behavior exists across vertebrates.
KeywordsAndrogen receptor Testosterone Sexual selection Signal evolution Frogs
Supported by NSF IOS-1655574 to L.A.M and M.J.F. All animal experiments that are the authors’ original work have been approved by the IACUC of Smith College and Wake Forest University.
- Adkins-Regan E (2005) Hormones and animal social behavior. Monographs in behavior and ecology. Princeton University Press, PrincetonGoogle Scholar
- Ball GF (2003) Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. In: Hauser M, Konishi M (eds) The design of animal communication. Cambridge, pp 213–253Google Scholar
- Boistel R, Sueur J (2002) Female calls among amphibian anura: an exceptional sound behavior? Bioacoustics 13:80–81Google Scholar
- Fuxjager MJ, Miles MC, Goller F, Petersen J, Yancey J (2017) Androgens enhance male acrobatic courtship by enhancing muscle speed and easing the severity of its trade-off with force. Endocrinology. doi: 10.1210/en.2017-00599
- Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian, Washington DCGoogle Scholar
- Mangiamele LA, Fuxjager MJ, Schuppe ER, Taylor RS, Hödl W, Preininger D (2016) Increased androgenic sensitivity in the hind limb muscular system marks the evolution of a derived gestural display. Proc Natl Acad Sci USA 113:5664–5669. doi: 10.1073/pnas.1603329113 CrossRefPubMedPubMedCentralGoogle Scholar
- Nelson RJ (2000) An introduction to behavioral endocrinology, 2nd edn. Sinauer Associates, Inc., SunderlandGoogle Scholar
- Preininger D, Weissenbacher A, Wampula T, Hödl W (2012) The conservation breeding of two foot-flagging frog species from Borneo, Staurois parvus and Staurois guttatus. Amphib Reptile Conserv 5:45–56Google Scholar
- Preininger D, Handschuh S, Boeckle M, Sztatecsny M, Hödl W (2016) Comparison of female and male vocalisation and larynx morphology in the size dimorphic foot-flagging frog species, Staurois guttatus. Herpetol J 26:187–197Google Scholar
- Searcy WA, Nowicki S (2005) The evolution of animal communication. Princeton University Press, PrincetonGoogle Scholar
- Zornik E, Kelley DB (2017) Hormones and vocal systems: insights from Xenopus. In: Pfaff D, Joëls M (eds) Hormones, brain, and behavior, vol 2, 3rd edn. Elsevier, Amsterdam, pp 117–144Google Scholar