Insight into the neuroendocrine basis of signal evolution: a case study in foot-flagging frogs

Abstract

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.

A Common Endocrine Signature Marks the Convergent Evolution of an Elaborate Dance Display in Frogs

“…Importantly, such a relationship is not evident in the nervous system, a finding that is contrary to past work that indicates that gross measures of AR in the CNS are similarly higher in taxa that produce highly elaborate gestural displays (Feng et al 2010;Fuxjager et al 2012). Accordingly, we hypothesize that elevated AR in the thigh muscles is an adaptive trait, given that androgenic activation of these receptor populations likely promotes foot-flagging behavior when males compete for access to female mates and resources (Mangiamele et al 2016;Mangiamele and Fuxjager 2018). Selection for foot-flagging may therefore proceed in unrelated taxa by driving similar specializations to the endogenous androgenic system of specific tissues within the body.…”

Comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'

“…An alternative view, however, is that these so-called “spontaneous” limb movements are actually generated as social signals that help males compete with sexual rivals during agonistic interactions. Most frogs that use gestural signals do so for this purpose (see Table 1 ), and thus the behavior is assumed to evolve through intrasexual selection ( Preininger et al, 2013b ; Preininger et al, 2013c ; Mangiamele and Fuxjager, 2018 ; Anderson et al, 2021a ). Zhao et al do not determine how many of the limb movements produced in the absence of parasites (e.g., “spontaneous”) were actually the result of male-male interactions, but they do indicate that little torrent frogs use these movements in such contexts.…”

Genome assembly of the foot-flagging frog, Staurois parvus: a resource for understanding mechanisms of behavior

“…Together, this indicates that protein evolution is also a plausible mechanism contributing to the emergence of foot-flagging behavior, as has been previously predicted ( Mangiamele et al . 2016 ; Mangiamele and Fuxjager 2018 ). Further analysis of AR sequence, potentially in combination with full-length isoform sequencing, will be particularly informative in this system.…”