Deep‐Time Convergent Evolution in Animal Communication Presented
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Received: 18 November 2020 | Revised: 15 April 2021 | Accepted: 19 April 2021 DOI: 10.1111/ele.13773 LETTER Deep- time convergent evolution in animal communication presented by shared adaptations for coping with noise in lizards and other animals Terry J. Ord1 | Danielle A. Klomp1 | Thomas C. Summers1 | Arvin Diesmos2 | Norhayati Ahmad3 | Indraneil Das4 1Evolution & Ecology Research Centre Abstract and the School of Biological, Earth and Environmental Sciences, University of New Convergence in communication appears rare compared with other forms of ad- South Wales, Sydney, NSW, Australia aptation. This is puzzling, given communication is acutely dependent on the envi- 2Herpetology Section, Zoology Division, National Museum of the Philippines, ronment and expected to converge in form when animals communicate in similar Manila, Philippines habitats. We uncover deep- time convergence in territorial communication between 3Department of Biological Sciences and Biotechnology, Universiti Kebangsaan two groups of tropical lizards separated by over 140 million years of evolution: Malaysia, Bangi, Malaysia the Southeast Asian Draco and Caribbean Anolis. These groups have repeatedly 4Institute of Biodiversity and Environmental Conservation, Universiti converged in multiple aspects of display along common environmental gradients. Malaysia Sarawak, Kota Samarahan, Malaysia Robot playbacks to free- ranging lizards confirmed that the most prominent con- vergence in display is adaptive, as it improves signal detection. We then provide Correspondence Terry J. Ord, Evolution & Ecology evidence from a sample of the literature to further show that convergent adap- Research Centre and the School of Biological, Earth and Environmental tation among highly divergent animal groups is almost certainly widespread in Sciences, University of New South Wales, nature. Signal evolution is therefore curbed towards the same set of adaptive solu- Sydney, NSW, Australia. Email: [email protected] tions, especially when animals are challenged with the problem of communicating Funding information effectively in noisy environments. University of New South Wales (UNSW) KEYWORDS Editor: Greg Grether adaptive differentiation, contextual plasticity, historical contingency, repeated evolution, robotic playbacks INTRODUCTION common communicative strategies does not appear to be as likely as convergence in morphology (Ord & Animals relying on signals for similar functions— for Summers, 2015; York & Fernald, 2017; these two studies example, attracting mates or defending territories— and examined over 120 examples of convergent, parallel and trying to communicate under similar environmental functionally redundant adaptations repeatedly arising conditions are expected to converge in signal character- from independent evolution). This is despite behaviour istics (Marler, 1967). This is because natural selection putatively being more evolutionarily labile than mor- should only favour those strategies that maximise the phology (Blomberg et al., 2003) and efficient communi- detection and recognition of communicative signals in cation being central to the reproductive fitness of many those environments (Endler, 1992). For example, com- animals (Bradbury & Vehrencamp, 2011). However, this munication theory (Dusenbery, 1992; Wiley, 2006) pos- could be because there are countless ways in which ani- its that animals should produce signals that maximise mals might maximise signal- to- noise ratios, making sig- the signal- to- noise ratio with the environment through nal convergence improbable. changes in the intensity of signalling or redundancy of Of the examples of convergence in animal communi- information conveyed. Yet the convergent evolution of cation, most are between populations of the same species 1750 | © 2021 John Wiley & Sons Ltd. wileyonlinelibrary.com/journal/ele Ecology Letters. 2021;24:1750–1761. ORD ET AL. | 1751 (Kemp et al., 2018; Ng et al., 2013) or taxa that are other- irrespective of the length of time taxa have evolved inde- wise closely related (Henry et al., 1999; Ord et al., 2013b). pendently of one another. This in itself is not unusual for adaptive convergence To help resolve the issue, we examined lizards from (Ord & Summers, 2015; Vermeij, 2006). It could reflect the Old World iguanians (the family Agamidae) and New adaptive outcomes being predisposed along common World equivalent (the family Iguanidae) that rely heav- evolutionary trajectories because of shared genetic and ily on vision for social communication (Jenssen, 1977; developmental pathways between closely related taxa Ramos & Peters, 2016). In these families, visual signals (Conte et al., 2012; Stern, 2013; these two studies exam- are vital for male lizards to establish and maintain terri- ined over 40 cases of parallel evolution— i.e., instances of tories (Jenssen et al., 2012; Ord, 2008). Signals are usually similar outcomes evolving independently through com- centred on the performance of an elaborate sequence of mon genetic pathways). It might also reflect a systematic head and body movements that convey reliable cues on bias in studies being skewed towards documenting con- physical condition (Brandt, 2003; Perry et al., 2004) and, vergence in closely related taxa (Ord & Summers, 2015). subsequently, their potential ability to aggressively de- This is an issue for our general understanding of the fend territory (van Dyk & Evans, 2008). The detection of adaptive process, as it remains unclear whether a mul- lizard territorial displays is also known to be acutely de- titude of adaptive solutions exists for the same selection pendent on the properties of the environment. Previous pressure— with adaptations only tending to converge work on male iguanid Anolis lizards in the Caribbean among closely related taxa— or whether natural selec- has shown that the speed (intensity) and duration (re- tion repeatedly produces the same set of adaptations dundancy) of territorial displays are contextually plastic within some species (Table 1), and evolutionary differen- tiated across species, as a function of habitat light and TABLE 1 Glossary of terms background visual noise generated by windblown vege- Term Definition tation (Ord et al., 2010a, 2016). This is an adaptive out- come predicted by communication theory (Dusenbery, Contextual plasticity Reversible changes in behaviour in 1992; Wiley, 2006). response to fluctuations in external environmental stimuli (see Stamps & It is unknown, however, whether the distantly re- Groothuis, 2010). This has also been lated species of the agamid family have converged on referred to as ‘activational plasticity’ the same signal strategies in response to the same en- (Snell- Rood, 2013) and ‘reversible vironmental conditions. An informal comparison be- phenotypic plasticity’ (Wright & tween the Caribbean iguanid Anolis lizards (Ord et al., Turko, 2016) 2010a) and some Australian and Chinese agamid species Contextual reaction Behaviour described by the regression norm line computed from the response of (Peters et al., 2007; Peters et al., 2016; Ramos & Peters, behaviour to external environmental 2017a) suggests this is not the case. However, the ecol- stimuli. The slope of the line reflects ogy of these particular agamid species is fundamentally the contextual plasticity of behaviour different from the iguanid Anolis, making the compari- as a function of fluctuations in son problematic. These agamids communicate in open, environmental stimuli, whereas the intercept of the line represents the sunny environments and from locations close to (or on) ‘baseline’ behaviour that would be the ground, where the visual environment is likely to be expected at a specific value of the quite different to the arboreal, and often forested, envi- environmental stimuli ronments occupied by the Anolis lizards. Visual noise Within- taxon The ‘baseline’ behaviour that would from windblown vegetation does appear to be a mask- intercept be observed under a standard ing agent for the displays of at least one agamid species environmental condition, specifically (Peters, 2008), but these lizards rely on an intermittent when the external stimulus affecting behaviour has a value of zero. This series of rapid tail flicks for enhancing detection (Peters intercept value can be used to identify et al., 2007), a behaviour unlike anything seen in the the portion of behaviour that is not iguanid lizards (including Anolis). More generally, the contextually plastic and potentially repertoire of signal components used in territorial ad- the product of evolutionary vertisement display— and that could be modified to im- differentiation (see Ord et al., 2010a) prove detection in visually difficult conditions— differs Within- taxon mean The average phenotypic value (e.g., between the iguanids and agamids, at least on first ex- behaviour) or average environmental value (e.g., ambient light) exhibited or amination (presented below). experienced by individuals of a given On the opposite side of the world to the Caribbean taxon iguanid Anolis lizards, and separated by over 140 mil- Within- taxon slope The average contextual plasticity lion years of divergent evolution history (Kumar et al., expressed by individuals of a given 2017), are the Southeast Asian agamid Draco lizards taxon in response to fluctuations in (Figure 1). Unlike other agamid groups, Draco is a re- external environmental stimuli markable ecological analogue to the Anolis. Although DEEP- TIME CONVERGENT EVOLUTION IN ANIMAL COMMUNICATION PRESENTED