When Does Sexual Signal Exploitation Lead to Signal Loss?

Abstract

Evolutionary loss of traits is common over evolutionary time and occurs in diverse taxa. Sexual signals and other non-signal traits should differ in their likelihood of becoming lost because they experience different selection pressures contributing to their diminution or persistence. In particular, conspicuous sexual signals are often exploited by natural enemies; this significant cost can favor signal reduction or loss. Yet sexual signals should also experience strong selection favoring their persistence because they facilitate communication during sexual encounters and their loss would involve changes in both the signaler and receiver. Most examples of sexual signal loss come from phylogenetic studies, so it is difficult to ascertain the context and key factors responsible for their loss. Here, we describe one of the best documented examples of evolutionary sexual signal loss in real time due to signal exploitation: Teleogryllus oceanicus (the Pacific field cricket) in Hawaii where many males have lost the ability to sing due to natural selection from a deadly, acoustically-orienting parasitoid fly. Using sexual signal loss in T. oceanicus as a model, we identify environmental, social, and genetic factors that appear generally important in driving sexual signal loss due to signal exploitation. We also discuss each putative factor contributing to signal loss more broadly within the context of non-signal trait loss. Overall, the factors that facilitate evolutionary loss of signals and other traits exhibit significant parallels. In general, a significant cost from the environment, weak selection for persistence, and alternative ways of accomplishing the former function appear critical to achieving evolutionary loss of both sexual signals and non-signal traits. However, because few empirical examples of sexual signal loss over contemporary timescales exist, we need more theory and empirical work to better understand the evolutionary dynamics of sexual signal loss.

Sexual signal loss, pleiotropy, and maintenance of a male reproductive polymorphism in crickets

“…However, because most evidence is from phylogenies, it is difficult to study how sexual signal loss evolves in real time (Wiens 2001). For a signal to become lost, some type of cost must select for its diminution (Heinen‐Kay and Zuk 2019). Many sexual signals are costly because they attract attention from predators and parasites (Tuttle and Ryan 1981; Zuk and Kolluru 1998; Godin and McDonough 2003; Heinen‐Kay et al.…”

“…2004; Kemp 2008). Although such costs can certainly promote signal reduction, they rarely appear to drive the complete loss of a sexual signal on their own (Heinen‐Kay and Zuk 2019). Theory and empirical work suggests that a significant reduction or complete absence of selection favoring the trait is also necessary for signal loss to evolve (Morris et al.…”

“…2005; Weigel et al. 2015; Heinen‐Kay and Zuk 2019). Under certain circumstances, female choosiness itself can become costly, independent of selection on the signal, thereby favoring a weakening of female mating preferences (Kaneshiro 1976, 1980).…”

Signaler–receiver–eavesdropper: Risks and rewards of variation in the dominant frequency of male cricket calls

“…That is, there is often a trade‐off between the cost of a mating signal trait and the benefit of that trait for increased reproduction (e.g., Heinen‐Kay et al., 2014). Net stabilizing selection can be disrupted by changes to the strength of natural and/or sexual selection: Male signal traits can become more elaborated under low predation regimes (e.g., Endler, 1980) or conversely they can be lost entirely with dramatically increased predation pressure (e.g., Heinen‐Kay & Zuk, 2019; Zuk et al., 2006). Males may also change how much they signal (Cade, 1984) and/or when they signal (Bertram et al., 2004) in response to predators.…”

“…or conversely they can be lost entirely with dramatically increased predation pressure (e.g., Heinen-Kay & Zuk, 2019;Zuk et al, 2006).…”