Trait duplication by means of sensory bias

Trait duplication has played an important role in the origin of species, higher taxonomic groups, and novel traits (WestEberhard 2003; Carroll 2005; Lynch 2007; Leitch AR and Leitch IJ 2008; Mondragón-Palomino and Theiben 2008). Trait duplication involves the duplication of body segments, body parts, genes, and even of whole genomes. These events can promote diversification and novelty by allowing previously evolved mechanisms to acquire novel functions, rather than requiring the machinery for those novel functions to be selected from scratch, mutation by mutation (West-Eberhard 2003; Carroll 2005; Lynch 2007; Des Marais and Rausher 2008). I suggest that a well-known mechanism in behavioral ecology—sensory bias—may foster a process resulting in trait duplication with important consequences for the diversification of mate preferences. Sensory bias is a process in which preferences originate when responses that evolved in nonsexual contexts or as by-products of sensory systems or other preferences are co-opted by novel displays into favoring as mates the individuals that use the displays (West-Eberhard 1984; Ryan 1990, 1998; Arak and Enquist 1993; Christy 1995; Endler and Basolo 1998; ten Cate and Rowe 2007; Vahed 2007). For example, responses that evolved in ecological contexts may be co-opted, as in water mites in which a predatory response is elicited by a male display (Proctor 1991, 1992). Work with diverse taxa suggests that co-option by sensory bias is often involved in the origin of preferences (West-Eberhard 1984; Endler and Basolo 1998; Rodrı́guez and Snedden 2004; Gerhardt et al. 2007; Vahed 2007). This process has received various terms—for example, sensory trap, sensory exploitation, preexisting bias— emphasizing different aspects of selection on responses and having different implications for the subsequent evolution of the preference (Endler and Basolo 1998). Furthermore, sensory bias may refer to a feature of the sensory system, to the process of co-option (Ryan 1990), to a product of selection, or to a by-product feature (Arak and Enquist 1993; Endler and Basolo 1998; Arnqvist 2006). Here, I address processes in which a fully formed trait is co-opted either from a different context or from a different range of display values. I refer to the process of co-option as ‘‘co-option by sensory bias’’ and to the response as the ‘‘co-opted response. ’’ Co-option by sensory bias has 2 major consequences, each apparently at odds with the other: 1) It can incorporate a great diversity of traits and modalities of perception into sexual selection (West-Eberhard 1984; Christy 1995; Sakaluk 2000; Arnqvist 2006; Vahed 2007). With traits co-opted from ecological contexts, this amounts to ‘‘ecological capture’’ of diversity (to paraphrase the hypothesis of genic capture in sexual traits; Rowe and Houle 1996). But even with by-products of sensory systems, co-option also enriches the variety of preferences and displays. Sensory bias may thus help fuel rapid and extravagant evolution by sexual selection (West-Eberhard 1983, 1984). 2) However, the long-term course of this process is contested, with considerable debate about the capacity of a co-opted response to coevolve and diverge with a display (Ryan 1990, 1998, 1999; Reeve and Sherman 1993; Ryan and Rand 1993; Basolo and Endler 1995; Christy and Backwell 1995; Shaw 1995; Sherman and Wolfenbarger 1995a, 1995b; Endler and Basolo 1998; Sherman and Reeve 1999; Autumn et al. 2002; Rodrı́guez and Snedden 2004; Fuller et al. 2005; Arnqvist 2006; Kokko et al. 2006). Nevertheless, there are cases in which it seems that coevolution has followed co-option. For example, moth hearing evolved under selection to evade bat echolocation cries, and in some species it then evolved a function in pair formation involving approach to ultrasonic signals (Greenfield 2002). If initial responses were negative, coevolution must have followed because current sexual responses are positive (Bradbury and Vehrencamp 1998, p. 533). However, it is not clear what mechanisms fostered this trajectory, although categorical perception (Greenfield and Weber 2000; Greenfield and Baker 2003; Greig and Greenfield 2004) and context-dependence (Rodrı́guez and Greenfield 2004) help regulate current responses. The challenge presented by sensory bias is thus to understand the evolution of a co-opted response after co-option.