Communication theory and the form of receiver-mediated selection

Schaefer, H.M. and Ruxton, G.D. (2010) Communication theory and the form of receiver-mediated selection. Trends in Ecology and Evolution, 25(7), pp. 383-384. (doi: 10.1016/j.tree.2010.04.003)

Abstract

In our article on the mechanisms underlying deception in plants we argued that the exploitation of perceptual biases (EPB) and mimicry represent two functionally distinct strategies that lead predictably to distinct degrees of resemblance with other objects. We proposed different scenarios for how both strategies are interrelated (Figure 2 and emphasised that they represent two parts of a continuum. In their reply, Schiestl et al. [2] emphasise the overall importance of EPB, suggesting that it is generally important in driving floral-trait evolution but unlikely to explain the particular case of the deception by rewardless flowers. We obviously agree that EPB can be an important mechanism in floral-trait evolution, but caution against assuming that it is the sole or pre-eminent driver.To evaluate the relative role of EPB, it is useful to compare its predictions on receiver-mediated selection to those expected by communication theory. EPB expects selection to be caused by open-ended preferences or by biases that are adaptive in another context [3], whereas communication theory posits that stimuli are selected according to their detectability and their content [4]. The few studies that have examined the relationship between stimulation of the receiver and surrogates of plant fitness do not support open-ended preferences. Instead, the number of fruits detected by the guild of frugivorous birds in a tropical community follows an asymptotic function of fruit conspicuousness [5], demonstrating that the efficacy of fruit visual stimuli cannot be enhanced above a certain threshold. This result is inconsistent with the EPB model but explicable by the core tenet of signal theory that selection for increased conspicuousness can drive the evolution of communicative traits. The crucial difference is that selection for increased conspicuousness is sigmoid, driven by the signal-to-noise ratio and thereby contingent on the environment. Conversely, selection is primarily dependent upon the inherent biases of receivers according to EPB. Given the ubiquity of selection for increased conspicuousness in communication systems [4], this form of receiver-mediated selection should be an appropriate null model against which to compare the relative importance of EPB in floral-trait evolution.Plants could exploit pollinator biases that are adaptive in another context. Schiestl [6] provides a good case that EPB could explain the evolution of floral scent. However, evidence for adaptive colour biases is rare, and colour preferences are usually transient and inconsistent among individuals [7]. In contrast to the assertion of Schiestl et al. [2], the convergent evolution of red colouration in bird-pollinated flowers is not easily understood by adaptive biases because the plumage of pollinators (hummingbirds, honeyeaters, and sunbirds) is not predominantly red. Instead, it is explicable by signal theory because red is a particularly contrasting colour for birds [8]. The currently limited evidence for adaptive biases cautions against assuming that they generally drive floral evolution.Schiestl et al. argue that, by focussing on receiver-mediated selection as a possible driver of deception, we confuse proximate with ultimate mechanisms. We certainly agree that higher outcrossing rates, as they suggest, can contribute to explaining the evolution of rewardless flowers. Yet, it is obviously important to consider all costs and benefits associated with alternative strategies. Again, communication theory provides a framework for evaluating aspects related to communicating with animals. For example, in poison frogs, increasing conspicuousness or toxicity affords equivalent avoidance by predators and provides protection for non-toxic mimetic species [9]. By analogy, plants can achieve successful pollination and seed dispersal by increasing the conspicuousness or the information content of communicative traits. The information content refers to the reliability of indicating nutritional rewards. Both signalling strategies occur in fruits where conspicuous colours are unrelated to fruit nutritional contents, whereas less conspicuous colours indicate fruit rewards [10]. This dichotomy in advertising suggests that augmenting conspicuousness can be a precursor for the evolution of deception in plants. In this scenario, the paradox alluded to by Schiestl et al. (that experimental addition of nectar leads to higher pollination success of unrewarding plants) is a logical consequence of combining two successful advertising strategies: high conspicuousness and high nutritional rewards. We therefore emphasise that the costs and benefits of alternative phenotypes of floral appearance can arise in distinct contexts, including signalling. As such, EPB and communication theory should be useful frameworks for understanding the evolution of deception.

• Item Type: Articles
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Ruxton, Professor Graeme
• Authors: Schaefer, H.M., and Ruxton, G.D.
• College/School: College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: Trends in Ecology and Evolution
• ISSN: 0169-5347