Evolutionary novelty in communication between the sexes

Abstract

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.

Keywords: animal communication; environmental change; receiver; sender; sexual selection; signal.

Figure 1.

Novelty in animal signals and receiver features: (i) Odorrana tormota evolved ultrasonic calling songs, while ancestral species' songs are audible [2]; picture credit: A.S. Feng (https://phys.org/news/2008-05-female-concave-eared-frogs-ultrasonic.html); (ii) recently evolved morphs of the Pacific field cricket (Teleogryllus oceanicus) produce new sexual signals using modified wing morphology ([3]; picture credit: E.D. Broder); (iii) coevolution between male signals and female preference functions across the Enchenopa binotata complex [4]; picture credit: R.L. Rodríguez; (iv) in Drosophila, temperature impacts sender signalling behaviour but has minimal effects on female preferences [5]; picture credit: Hannah Davis/CC BY-SA (https://creativecommons.org/licenses/by-sa/4.0); (v) vervet monkeys use blue scrotal colour in sexual communication, which differs among species [6]; picture credit: Bjørn Christian Tørrissen/CC BY-SA (https://creativecommons.org/licenses/by-sa/3.0); (vi) visual signal variation in closely related Habronattus (top; picture credit Marshal Hedin) and Maratus (bottom; picture credit Madeline Girard) jumping spiders [7]; (vii) A. Origin of female foraging bias for male terminal yellow bands. B. Origin of terminal yellow band in males. C. Origin of female resistance to foraging costs in goodeid fishes [8]; picture credit: Wolfgang Gessl; (viii) satin bower birds (Ptilinorhynchus nuchalis) incorporate discarded blue items like pens, clothespins and bottlecaps into their displays [9,10]; picture credit: Gail Hampshire CC BY 2.0; (ix) frequency characteristics of vocal songs (produced via the syrinx) and feather sounds (produce via aeroelastic flutter) are similar across the ‘bee’ hummingbird clade ([11]; picture credit: Anand Varma); (x) electric mating signals have evolved independently in multiple lineages including elephant fish (Paramormyrops spp.) [12]; picture credit: C. Hopkins (https://www.nature.com/articles/467159a).

Figure 2.

Simplified schematic showing alternative scenarios by which novelty may evolve in mating communication. Our example is a generalized peacock Jumping spider (Maratus spp.) mating system where drab females choose males based on many traits including abdomen colouration. Change is initiated by mechanisms including mutation, hybridization, plasticity and cultural innovation. If change is in a signal component only, scenario 1 follows. If change is in a receiver feature only, scenario 2 unfolds. Change may be simultaneously initiated in both sender and receiver and if compatible, scenario 3 follows. Scenario 4 occurs when environmental change approximates signal change (left) or receiver change (right). In this example, there is a change in the light environment. Blue boxes indicate proximate considerations, while green indicate ultimate considerations. Glasses on the receivers represent receiver features (i.e. sunglasses indicating monochromatic and 3D red/blue glasses indicating colour vision). There are some simplifications here. For instance, in all scenarios, new signal components and receiver features may not be costly and could be maintained in the genome and later co-opted for a communication function. Additionally, new traits are subject to costs and benefits, including those unrelated to mating communication, and we should expect them to persist only when net benefits outweigh costs.