Abstract

Alarm signals released after predator attack function as reliable public information revealing areas of high risk. The utility of this information can extend beyond species boundaries, benefiting heterospecifics capable of recognizing and responding appropriately to the signal. Nonmutually exclusive hypotheses explaining the acquisition of heterospecific reactivity to cues suggest it could be conserved phylogenetically following its evolution in a common ancestor (a species‐level effect) and/or learned during periods of shared risk (a population‐level effect; e.g., shared predators). Using a laboratory‐based space‐use behavioral assay, we tested the response of sea lamprey (Petromyzon marinus) to the damage‐released alarm cues of five confamilial (sympatric and allopatric) species and two distantly related out‐groups: a sympatric teleost (white sucker Catostomus commersonii) and an allopatric agnathan (Atlantic hagfish Myxine glutinosa). We found that sea lamprey differed in their response to conspecific and heterospecific odors; exhibiting progressively weaker avoidance of cues derived from more phylogenetically distant confamilials regardless of current overlap in distribution. Odors from out‐groups elicited no response. These findings suggest that a damage‐released alarm cue is at least partially conserved within the Petromyzontidae and that sea lamprey perceives predator attacks directed to closely related taxa. These findings are consistent with similar observations from gastropod, amphibian and bony fish taxa, and we discuss this in an eco‐evo context to provide a plausible explanation for the acquisition and maintenance of the response in sea lamprey.

Highlights

  • Predation and the recognition of predation risk can be powerful selective forces, capable of shaping interactions within and among predators and prey as they seek to gain advantage in this lethal contest (Dawkins & Krebs, 1979; Genovart et al, 2010)

  • The strength of response to damage-­released alarm cues declined in close association with increasing phylogenetic distance between sea lamprey and other lamprey species from which alarm cues were derived

  • By testing alarm cues of representatives from 50% of Petromyzontidae genera, including the most basal sister group (Ichthyomyzon–Petromyzon, Gill, Renaud, Chapleau, Mayden, & Potter, 2003), our results suggest that the components of the damage-­released alarm cue in sea lamprey are at least partially conserved within the northern hemisphere lampreys

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Summary

| INTRODUCTION

Predation and the recognition of predation risk can be powerful selective forces, capable of shaping interactions within and among predators and prey as they seek to gain advantage in this lethal contest (Dawkins & Krebs, 1979; Genovart et al, 2010). Several aquatic taxa avoid heterospecific alarm cues, often exhibiting a decline in the intensity of antipredator behavior with increasing phylogenetic distance between the individual attacked and the individual perceiving that event (Dalesman et al, 2007; Hazlett & McLay, 2005; Mitchell, Cowman, & McCormick, 2012; Schoeppner & Relyea, 2009) One explanation for this pattern is that individuals innately recognize the damage-­released alarm cues of closely related taxa because they were present in a common ancestor (i.e., are chemically similar). Over evolutionary time, gradual changes to these chemical compounds responsible for initiating antipredator behaviors result in only partial recognition of the cue, regardless of whether both species continue to overlap spatially and share predators This explanation has been previously referred to as the “phylogenetic-­relatedness hypothesis” (Schoeppner & Relyea, 2009). If the phylogenetic-­relatedness hypothesis applies, we expected the intensity of avoidance of extracted lamprey alarm cues would diminish with phylogenetic distance

| MATERIALS AND METHODS
Findings
| DISCUSSION
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