Female sea lamprey shift orientation toward a conspecific chemical cue to escape a sensory trap

Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2016), 27(3), 810–819. doi:10.1093/beheco/arv224 Original Article Female sea lamprey shift orientation toward a conspecific chemical cue to escape a sensory trap Cory O. Brant, Nicholas S. Johnson, Ke Li, Tyler J. Buchinger, and Weiming Li Department of Fisheries and Wildlife, Michigan State University, Room 13 Natural Resources Building, 480 Wilson Road, East Lansing, MI 48824, USA Received 31 July 2015; revised 23 November 2015; accepted 27 November 2015; Advance Access publication 20 December 2015. The sensory trap model of signal evolution hypothesizes that signalers adapt to exploit a cue used by the receiver in another context. Although exploitation of receiver biases can result in conflict between the sexes, deceptive signaling systems that are mutually beneficial drive the evolution of stable communication systems. However, female responses in the nonsexual and sexual contexts may become uncoupled if costs are associated with exhibiting a similar response to a trait in both contexts. Male sea lamprey (Petromyzon marinus) signal with a mating pheromone, 3-keto petromyzonol sulfate (3kPZS), which may be a match to a juvenile cue used by females during migration. Upstream movement of migratory lampreys is partially guided by 3kPZS, but females only move toward 3kPZS with proximal accuracy during spawning. Here, we use in-stream behavioral assays paired with gonad histology to document the transition of female preference for juvenile- and male-released 3kPZS that coincides with the functional shift of 3kPZS as a migratory cue to a mating pheromone. Females became increasingly biased toward the source of synthesized 3kPZS as their maturation progressed into the reproductive phase, at which point, a preference for juvenile odor (also containing 3kPZS naturally) ceased to exist. Uncoupling of female responses during migration and spawning makes the 3kPZS communication system a reliable means of synchronizing mate search. The present study offers a rare example of a transition in female responses to a chemical cue between nonsexual and sexual contexts, provides insights into the origins of stable communication signaling systems. Key words: mate search, olfaction, Petromyzon marinus, pheromone, sensory bias. INTRODUCTION The sensory trap model of signal evolution hypothesizes that males exploit an existing female preference for a cue in a nonsexual context by signaling with that trait during reproduction (Ryan and Cummings 2013). Although exploitation of a receiver bias can result in conflict between the sexes if optimal reproductive decisions differ, deceptive signals that are mutually beneficial can drive the evolution of stable communication systems (Garcia and Ramirez 2005). Females that overcome the deception and adjust their responses are selected for if a cost is associated with responding similarly in both the nonsexual and sexual contexts (Stuart-Fox 2005; Garcia and Lemus 2012). Although many empirical studies implicate a role of sensory traps underlying female preference for male signals (reviewed by Ryan and Cummings 2013), transitions associated with uncoupled responses in the nonsexual and sexual contexts remain poorly documented. Address correspondence to W. Li. E-mail: . N.S.J. Coauthor is now at USGS, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI 49759, USA © The Author 2015. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: Chemical communication is a widely employed sensory modality that offers opportunity to examine the evolution of signaling systems (Christy and Rittschof 2011). Previous research on the evolution of animal communication systems has focused primarily on visual and vocal stimuli (Christy 1995; Tibbetts 2002; Hurd and Enquist 2005; Stoddard and Prum 2011; Gasparini et al. 2013; Kelley LA and Kelley JL 2014), perhaps because they are often within the range of human perception. The evolution of chemical signals remains poorly understood (Symonds and Elgar 2008; Wisenden 2014), but some signals are hypothesized to be cues that have become exaggerated (Christy and Rittschof 2011; Wisenden 2014). For example, stimuli can originate as by-products of physiological processes such as “leaking” of hormones or metabolites, or secretion of cuticular defensive or protective compounds (Døving et al. 1980; Christy and Rittschof 2011; Davidson et al. 2011; Weiss et al. 2013). Detection of chemical stimuli can be used to make decisions through adaptations in receivers (chemical cues) or both receivers and signalers (chemical signals; Wyatt 2011). Recent phylogenetic comparisons indicate that female orientation toward a compound used as a mating pheromone in sea lamprey Brant et al. • Female sea lamprey shift orientation (Petromyzon marinus) transitions between nonsexual and sexual contexts (Buchinger et al. 2013). Sea lamprey utilize pheromones to modulate key aspects of their life history. Pheromones are discussed here as chemical signals that are produced by an organism and elicit a physiological or behavioral response in conspecifics (Karlson and Lüscher 1959). Adult sea lampreys cue onto odors of stream-residing juvenile larvae to navigate toward suitable spawning habitat during their springtime migration from freshwater lakes, or the Atlantic Ocean, into freshwater streams (Teeter 1980; Bjerselius et al. 2000; Wagner et al. 2009). Males typically move upstream before females (Applegate 1950), establish nests (Manion and Hanson 1980), and, on sexual maturation, release a bile salt known as 3-keto petromyzonol sulfate (3kPZS) that functions as a sex pheromone (Li et al. 2002; Siefkes et al. 2005; Johnson et al. 2006, 2009). Female sea lamprey preference for 3kPZS is hypothesized to have originated in a nonsexual context (Buchinger et al. 2013). Female silver lamprey (Ichthyomyzon unicuspis), a close relative of sea lamprey, exhibit an upstream migratory response to 3kPZS but only streamresident juveniles and not sexually mature males release 3kPZS into the water (Buchinger et al. 2013). In sea lamprey, general upstream movement of males and females is initiated by 3kPZS during migration (Brant et al. 2015) similarly to silver lamprey. However, unlike silver lamprey, female sea lamprey preference for 3kPZS appears to have been exploited by conspecific males, who dramatically upregulate the 3kPZS biosynthetic pathway (up to 8000-fold increase) in their livers (Yeh et al. 2012; Brant et al. 2013), and release 3kPZS at high rates (~0.5 mg/h) across specialized cells in the gill epithelia (Siefkes et al. 2003) on reaching sexual maturation. Although female preference for 3kPZS may have originated in a migratory context, the function of female orientation to conspecific odors dif (...truncated)