Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish

Behavioral Ecology doi:10.1093/beheco/arr119 Advance Access publication 11 July 2011 Original Article Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish Mate choice can vary in response to internal or external conditions that alter the costs and benefits of being choosy. The relationship between mate choice and hybridization, however, is not well understood. An important influence on mate choice is the rate at which potential mates are encountered: low rates increase sampling costs, favoring reduced choosiness. We investigated the influence of conspecific encounter rate on female choice in a naturally hybridizing species of swordtail, Xiphophorus birchmanni. We exposed females to conspecific males, followed by either no delay or a long (24 h) delay before their next male encounter. In this second encounter, females were offered the choice of a heterospecific (X. malinche) male only or a choice between a conspecific and heterospecific male. When not given a choice between 2 males, females spent more time with the heterospecific following a long delay between male encounters than after no delay, suggesting a decrease in choosiness. When offered a choice between males, however, females preferentially associated with the conspecific, regardless of the time between male encounters. These results suggest that females are sensitive to conspecific encounter rate but may employ a sample-based (vs. standard-based) comparison tactic, which could make hybridization less likely. We also found that, contrary to our expectations, females with only the heterospecific male to choose from visited him more frequently following a long delay between male encounters than following no delay, possibly indicating an increase in sampling effort. Our study highlights the potential importance of context-dependent mate choice in animal hybridization. Key words: encounter rate, hybridization, mate choice, mate density, sampling tactic, Xiphophorus. [Behav Ecol 22:1234–1240 (2011)] INTRODUCTION ndividuals can gain a variety of benefits from choosing among potential mates (Andersson 1994). Mate choice, however, is also costly, imposing time, energy, and/or survival costs on choosy individuals. The costs and benefits of mate choice depend on the chooser’s attributes and circumstance; as a result, variation in mate choice can arise in response to factors intrinsic to the chooser, such as age or experience (e.g., Kodric-Brown and Nicoletto 2001; Coleman et al. 2004), reproductive state (e.g., Lynch et al. 2005; Uetz and Norton 2007), condition (e.g., Burley and Foster 2006; Hebets et al. 2008; Holveck and Riebel 2010), as well as social and environmental factors including the quality (e.g., Kvarnemo and Simmons 1999), density (e.g., Shine et al. 2006), or familiarity of potential mates (e.g., Simcox et al. 2005), the operational sex ratio (e.g., Berglund 1994; Jirotkul 1999), competition for mates (e.g., Fawcett and Johnstone 2003), predation risk (e.g., Forsgren 1992; Hedrick and Dill 1993), habitat quality (e.g., Reynolds and Jones 1999; Hale 2008), and season (e.g., Qvarnström et al. 2000; Borg et al. 2006). In many species, individuals respond to changes in the costs and benefits of mate choice by adjusting their level of choosi- I Address correspondence to P.M. Willis. E-mail: pamwillis@utexas. edu. Received 16 November 2010; revised 9 May 2011; accepted 10 May 2011.
The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: ness, their mate preferences, their sampling strategy, or some combination thereof. For example, female fiddler crabs (Uca annulipes) become less selective as time constraints on successful reproduction increase (Backwell and Passmore 1996); female green swordtails (X. helleri) change their preference from long-sworded to short-sworded (less risky) males under greater perceived risk of predation (Johnson and Basolo 2003); and female pronghorns (Antilocapra americana) reduce their sampling effort, traveling shorter distances and visiting fewer males when they are in poorer condition (Byers et al. 2006). Typically, mate choice takes place among conspecifics; however, this is not always the case. The same dynamic conditions that produce variation in mate choice within species can also promote or inhibit mating among different species. For example, male western grebes (Aechmophorus occidentalis) increasingly pursue female Clark’s grebes (Ae. clarkii) as opportunities to pair with conspecifics decline over the breeding season (Nuechterlein and Buitron 1998), and female spadefoot toads (Spea bombifrons) become more permissive toward heterospecific (S. multiplicata) males when water levels are low, with low water levels giving the faster metamorphosizing hybrid tadpoles a higher chance of survival (Pfennig 2007). Such studies are uncommon but important because, as is becoming increasingly apparent, animal hybridization can be a significant source of evolutionary change, capable of promoting, inhibiting, or reversing diversification (Seehausen 2004; Mallet 2005, 2007). Identifying how mate choice inhibits or facilitates hybridization is therefore important to our understanding of how diversity is lost or gained. Pamela M. Willis,a Michael J. Ryan,a and Gil G. Rosenthalb Section of Integrative Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX 78712, USA and bDepartment of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA a 1235 An important influence on mate choice is the rate at which potential mates are encountered (reviewed in Jennions and Petrie 1997). Low encounter rates increase the costs of sampling, often resulting in a decline in choosiness (e.g., Alatalo et al. 1988; Milinski and Bakker 1992; Palokangas et al. 1992; Shelly and Bailey 1992; Berglund 1995). Among hybridizing species, low encounter rates might promote the acceptance of heterospecifics. Indeed, a scarcity of conspecifics is considered a common cause of hybridization (e.g., Mayr 1963), supported by the many observations of hybridization where one or both species are rare (e.g., Wirtz 1999; Randler 2002). The influence of conspecific encounter rate on heterospecific mate choice, however, has not been investigated experimentally in any species. Here, we investigate the influence of encounter rate on female mate choice in a naturally hybridizing species of swordtail, X. birchmanni. Xiphophorus fishes belong to the internally fertilizing live-bearing family Poeciliidae. The genus ranges from northeastern Mexico to Honduras, and many species occur in sympatry (Rauchenberger et al. 1990; Kallman and Kazianis 2006). Although there is little to no intrinsic postzygotic isolation between species (Rosen 1960; Kazianis et al. 1996; Kallman and Kazianis 2006), hybridization in the wild is uncommon (re (...truncated)