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Chapter 7
The Cue–Signal Continuum:
A Hypothesized Evolutionary
Trajectory for Chemical
Communication in Fishes
Brian D. Wisenden
Minnesota State University Moorhead, Moorhead, Minnesota, USA
7.1 Introduction
Chemical information is ubiquitous and can be a powerful releaser of behavioral responses (Sorensen
and Stacey, 1999; Wisenden and Chivers, 2006; Wyatt, 2010). Chemical information in the environment comes from abiotic and biotic sources. Abiotic cues allow fish to navigate to favorable habitat
along gradients in pH, dissolved oxygen, or salinity. Chemical cues of biotic origin are called
semiochemicals, after the Greek word semion for sign. Semiochemicals provide important
information to receivers about every aspect of physiological and ecological function, including
spatial and temporal variation in food availability, the diet choice of others, the identity of individual
group members on the basis of shared phylogeny, familiarity or kinship, the presence and activity of
predators, risk of parasitism, the dominance status of sexual rivals, and the location and reproductive
readiness of potential mates and cues that play a role in parent–offspring interactions (Bradbury and
Vehrencamp, 2011). The enormous fitness benefits of this information create selection pressure on
the sensory biology of fish to favor elaboration of receptors to detect this information and cognitive
processes to generate adaptive behavioral responses to this information. Wherever there is production of information by some individuals and exploitation of that information by other individuals,
there is also potential for co-evolutionary processes to shape both the sensory biology of receivers
to better detect these chemicals and for senders to specialize in production and release of semiochemicals (Stacey and Sorensen, 1991, Wisenden and Stacey, 2005, Wisenden and Chivers, 2006;
Stacey, 2015).
Odors, chemical cues and signals, signature mixtures, pheromones and “substances” are terms
used to describe the enormous diversity of semiochemicals that fish use to inform their behavioral
decision-making. The absence of universally accepted standard nomenclature has created confusion because these terms do not necessarily reflect the evolutionary underpinning involved in the
Fish Pheromones and Related Cues, First Edition. Edited by Peter W. Sorensen and Brian D. Wisenden.
© 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc.
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production, detection, and processing of this information. To fully understand their ecological
function, one needs an understanding of the evolutionary selection behind the origin and maintenance of semiochemical detection and production.
Historically, there have been two approaches to the study of fish semiochemicals: (1) by physiologists who study various aspects of the physiology and behavior of sex pheromones (e.g., Stacey and
Sorensen, 2009) and (2) by behavioral ecologists who study how chemical cues mediate predator-prey
interactions (e.g. Kelley, 2008; Ferrari, Wisenden, and Chivers, 2010). These parallel communities
of researchers have developed largely independent literatures, each with its own lexicon for semiochemicals. The best way for the study of semiochemicals in fishes to move forward is for there to be
integration of these literatures and with that an acceptance of a common vocabulary. Therefore, this
chapter aims at organizing known semiochemicals along a hypothesized evolutionary trajectory from
ancestral to derived. This framework will hopefully highlight opportunities for future research to fill
in gaps in collective knowledge and to test predictions of this hypothesis.
7.2 A HYPOTHESIS FOR THE EVOLUTION OF SEMIOCHEMICALS
Orientation → Contextualization → Specialization of production → Specialization of release
A plausible sequence for the evolution of use and production of several broadly defined classes of
semiochemicals (Table 7.1) is proposed here. The first and simplest form of behavioral response to
external chemical information is orientation. The simplest form of orientation occurs in response
to chemicals of abiotic origin, such dissolved oxygen, geological mineral cues and salinity, and so
on, which provide important information about the environment. Chemo-orientation is used in the
settlement of larvae of marine fishes, orientation cues for long-distance migratory behavior, and for
microhabitat use. These are not semiochemicals per se because semiochemicals are only those
chemicals that are released by living organisms.
Behavioral responsiveness to semiochemicals is a significant transition because it creates an opportunity for selection to act on the chemical nature of the cue itself. The simplest forms of semiochemicals
provide information about the presence of conspecifics (competitors, prospective mates) and heterospecifics (prey, predators, competitors). The second stage of evolution of semiochemicals is contextualization.
Semiochemicals become contextualized when they are reliably released during specific ecological or
physiological interactions. Context allows selection to shape behavioral responses in sophisticated ways.
Contextualized semiochemicals are still cues (i.e., not yet signals) because responses to semiochemicals
are driven entirely by selection on receivers. Receiver response to a chemical cue does not contribute to
fitness of the sender (Fig. 7.1). The first step toward elevating semiochemicals from cues to signals and,
thus, true chemical communication, is the elaboration of tissues specialized for production of messenger
chemicals, even if at first these chemicals are released for benefits other than manipulating receivers
(Wisenden and Stacey, 2005). The ultimate category of semiochemicals is when there is the elaboration
of tissues and behavioral mechanisms to produce and control release of specialized semiochemicals.
Examples from fishes can be described for each of these stages in the evolutionary trajectory
from chemical cues released passively as public information to chemical signals that are part of a
co-evolved communication system (Sorensen and Stacey, 1999; Wisenden and Stacey, 2005).
7.3 ORIENTATION TO ENVIRONMENTAL SEMIOCHEMICALS
The simplest, and presumably most ancestral, form of chemical cues that reveal information about
habitat suitability are chemicals that are released from the decay of organic matter and the geochemical makeup of the watershed, spatial and temporal variation in dissolved oxygen, and exposure to
salinity (e.g., Leggett, 1977; Kramer, 1987; Odling-Smee and Braithwaite, 2003; Maes, Stevens, and
Breine, 2007). An example of this phenomenon is diadromous fish that spend part of their life in
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The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical
Table 7.1. Summary of a hypothesis for the evolution of semiochemicals used by
fishes on the basis of the presence (1) or absence (0) of various selection pressures
on sender (S) and/or receiver (R). The Cue/signal transition to communication occurs
when senders show evidence of specialization for cue release.
Specialized issues
Semiochemical
Environmental cues
Environmental parameters
(pH, salinity, etc.)
Migratory cues (geochemistry)
Semiochemical cues
Food odors (amino acids)
Odor of prey, predator,
and conspecifics
Injury-released alarm cues
Recognition of familiarity
and kinship (signature mixtures)
Sex steroids
Semiochemical signals
(pheromones)
Bile acids
Conspecific cues about social
hierarchy
Sex pheromones
Selection on
Sender/
receiver
Biotic
Contextual
Production
Release
0
0
0
0
R
0
0
0
0
R
1
1
0
0
0
0
0
0
R
R
1
1
1
1
0
0
0
0
R
R
1
1
1
0
R
1
1
1
1
1
1
0/1
0/1
1
1
1
1
R/S + R
R/S + R
S + R
freshwater and part of their life in salt water. Anadromous salmonids mature in salt water and orient
to chemical cues of their natal streams during the migration back to freshwater to spawn (Scholz
et al., 1976), which include organics and odors from plant, animals, and amino acids from biofilms
(see Sorensen and Baker, 2015). Some catadromous fishes such as bull sharks spawn in salt water
and orient to low salinity gradients to find freshwater to grow to adulthood (Heupel and Simpfendorfer,
2008). Eels returning to freshwater orient to organic compounds released by biofilm organisms
(Sorensen, 1986, see Sorensen and Baker, 2015). The evolution of this kind of orientation results
from selection on receivers to elaborate receptors and neural wiring to detect and respond adaptively
to environmental chemicals of value to the fitness of the receiver (Table 7.1; Fig. 7.1).
7.4 Passively Released Biotic Semiochemicals without
Ecological Context
The sum of biochemical processes occurring within aquatic animals generates a chemical profile, that
is, a characteristic bouquet or mosaic of compounds that can uniquely identify the species (Sorensen
and Baker, 2015). These chemical profiles can also provide information about the internal state of the
animal such as hunger state, recent diet, and habitat use (Csanyi, 1985; Licht, 1989; Brown and Godin,
1999; Webster et al., 2007; Ferrari, Wisenden, and Chivers, 2010). Molecules are often passively
released from the mucus, gills, urine, and feces of fishes as a result of diffusion gradients and natural
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Fish Pheromones and Related Cues
Sender
Receiver
Semiochemicals
from sender
Production and release of
semiochemical
Physiological mechanisms
-
Hypertrophy of secretory tissues
Specialized gill cells
Conjugated steroids for release in urine
Bladder control
Ecological function
-
Species identification
Signal social status
Attract mates
Reproductiion
Differential reproductive success
- Promotion of genes for
Production of semiochemicals
Controlled released of semiochemicals
Response
Physiological mechanisms
Ecological function
- Olfactory receptor specificity, sensitivity
- Neural wiring
- Cognitive processing of information
-
Navigation
Find food
Avoid predators
Reproduction
Differential reproductive success
- Promotion of genes for
Detection of semiochemicals
Cognitive processing of chemical information
Figure 7.1. The evolution of signal production and release in senders and behavioral
responses to semiochemicals in receivers. In receivers, genes that give rise to the proximate
mechanisms of behavior (anatomical and physiological aspects of receptors, neural wiring
of cognitive processes—the capacity and inclination to behave) are promoted when an
individual responds adaptively to information contained in a semiochemical released into
the environment. The semiochemical provides information about the context and timing for
when a particular behavioral response will be most effective. When a response to
semiochemicals is executed at the correct time and in the correct place, it is effective in
achieving the ecological function (migration, foraging, predator avoidance, reproduction).
Responses to semiochemicals evolve when individuals that are best at exploiting chemical
information achieve greater reproductive success than individuals that do not respond as
adaptively to semiochemicals. Genes for the production and contextual release of
semiochemical signals by senders are promoted when the response of receivers confers a
fitness benefit to senders. In a co-evolved communication system, natural selection promotes
specialization for production and controlled release of the chemical signal (pheromone) to
make the signal more detectable to receivers whose responses benefit the sender.
metabolic clearance. Detection of these molecules in the chemical profile reveals presence/absence
information about specific organisms of fitness value to predators (odor of prey), to prey (odor of predators; Ferrari, Wisenden, and Chivers, 2010), species identification mating and migration (e.g. Scholz
et al., 1976; Fine and Sorensen, 2005; Sorensen et al., 2005; Keefer et al., 2006; Sorensen and Hoye,
2007), and settling site selection by larval coral reef fishes (Sweatman, 1988). Because these semiochemicals provide useful information, there is selection on receivers to detect and respond adaptively to
these semiochemicals. However, because senders do not benefit from the response of receivers, there is
no opportunity for selection to act on production of cues or control of their release (Fig. 7.1; Table 7.1).
7.5 Passive, Contextual Release of Semiochemicals
When release of semiochemicals occurs only during a limited range of ecological contexts, then
there will be opportunity for selection on receivers to tailor behavioral responses to those contexts.
For example, fish respond to semiochemicals released from damaged conspecifics (alarm cues) that
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are released when a predator damages prey tissues in the process of attack and consumption of prey
(Wisenden and Chivers, 2006; Kelley, 2008; Ferrari, Wisenden, and Chivers, 2010; Wisenden,
2015). Injury-released chemical cues are typically released only in the context of predation, and
therefore reliably indicate the presence of predation risk. Responses to alarm cues are innate. Labreared minnows show full response intensity to conspecific extract (e.g., Wisenden et al., 2010).
Fishes are also adept at detecting injury-released cues from injured conspecifics in the diet of unfamiliar predators (Mathis and Smith, 1993; Wisenden, 2015). Although the chemical nature of alarm
cues is not yet fully characterized for any species (Mathuru et al., 2012), there is no evidence
linking the source of alarm cues to a specialized structure for synthesis and release of an alarm cue.
Even the much-discussed epidermal club cells of Ostariophysi and Percid fishes (Smith, 1992) are
not directly linked to alarm cues (Chivers et al., 2007; Carreau-Green et al., 2008; Ferrari, Wisenden,
and Chivers, 2010).
Another example of a contextual semiochemicals is those released from familiar individuals (Ward,
Axford, and Krause, 2002, 2003; Ward and Hart, 2003; Ward, 2015). These cues are contextual because
they provide information in addition to the simple presence/absence of a conspecific. The ability to
discriminate familiar individuals leads to differential behavioral responses to these groups (Dugatkin
and Wilson, 1993; Ward and Hart, 2003; Ward et al., 2005; Webster et al., 2007). This class of semiochemical is considered a signature mixture by Wyatt (2010) because responses result from learning
either during a sensitive period early in development or based upon self-matching (e.g., Ward and Hart,
2003; Gerlach and Lysiak, 2006; Mehlis, Bakker, and Frommen, 2008; Le Vin, Mable, and Arnold,
2010; Green, Mirza, and Pyle, 2011; Ward, 2015).
Consistent with the types of semiochemicals discussed thus far in this chapter, information gathering of passively released contextual semiochemicals imposes selection pressure on receivers to
detect and respond adaptively to chemical information, but it does not exert any selection pressure on
senders to produce or regulate the release of semiochemicals.
7.6 Passive, Contextual Release from Tissues Specialized
for the Production of Semiochemicals
Chemical compounds that regulate internal physiological processes for cell–cell communication are
produced and secreted by specialized tissues and detected by specialized receptors on target tissues
within the same individual. Having specialized tissues to produce a chemical compound(s) is the first
step in interindividual chemical communication.
Bile is produced by specialized tissues in the liver, and many of the acids in bile are potent
odorants for which there is low-threshold olfactory sensitivity in many species, including bile
of conspecifics and heterospecifics (cross reactions among phylogenetically disparate species
of European eel, Anguilla anguilla; goldfish, Carassius auratus; and Mozambique tilapia,
Oreochromis mossambicus; Huertas et al., 2010). Adult sea lamprey (Petromyzon marinus) use
derivatives of larval bile acids as a migratory cue to find locations that contain larvae as an
indicator of suitable nursery habitat for spawning (Sorensen et al., 2005; Sorensen and Hoye,
2007; Fine and Sorensen, 2010).
In fishes, hormones produced by specialized tissues in the gonads regulate reproductive maturation. These hormones subsequently leak into the external environment where they reliably
inform nearby conspecifics of the reproductive status of that individual (Sorensen and Scott,
1994; Sorensen and Stacey, 1999). Studies on phylogenetically disparate fish taxa suggest that
hormonally based semiochemicals are more the rule than the exception (see Stacey, 2015). For
example, male tilapia, O. mossambicus, distinguish between preovulatory and postovulatory
females on the basis of chemical cues (Miranda et al., 2005). Redfin shiners (Notropis umbratilis)
spawn in the nests of green sunfish (Lepomis cyanellus). Spawning aggregations, territorial
behavior, and courtship by redfin shiners can be induced by chemical cues associated with gamete
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release (milt, ovarian fluids) of the host sunfish even when these cues are experimentally released
over substratum unsuitable for spawning (Hunter and Hasler, 1965). In this case, redfin shiners
exploit publicly released sexual cues of a heterospecific to cue the context and timing of their
own reproductive behaviors (Fig. 7.1). The absence of species specificity in these examples
underscores how conspecific exploitation of these same semiochemicals could lead to specialization to control the quantity and context of release, and thus the evolution of pheromonal systems
of communication.
Although there is once again selection on receivers to detect and respond adaptively to chemical
information, there is only incipient selection on senders to elaborate mechanisms of synthesis and
control of semiochemical release. Although the semiochemicals discussed thus far are passively
released by-products of endogenous physiological processes, they set the stage for the evolution of
specialized production and release of these cues because of the opportunity for receiver responses to
confer fitness benefits to senders. Control of release by senders is necessary if exploitation of semiochemical cues is to become a component of a co-evolved communication system where receivers
benefit from information in the semiochemical (and elaborate receptors and cognitive processes
to respond adaptively) and senders benefit from manipulating receivers (and elaborate mechanisms to
control production and release of the semiochemical signal).
7.7 Active, Voluntarily Released Chemical Compounds from
Tissues Specialized for Production, Storage, and Release
of Semiochemicals
There are several clear examples of hyperdeveloped (beyond the immediate needs of intercellular
communication) tissues for the synthesis and release of semiochemicals. Male sea lamprey possess
specialized glandular gill cells to facilitate the release of the bile acid-derived sex pheromone 7α,
12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (also known as 3keto-petromyzonol sulfate, or
3ketoPZS) (Li et al., 2002). Immunocytochemical experiments showed that 3ketoPZS is located in
cells in the interlamellar region of the gills of prespermiating males and moves to the gill lamellae
when males enter the spermiating phase of reproductive readiness (Siefkes et al., 2003).
Seasonal fluctuations in the size of the seminal vesicles in Clarias catfish coincide with the release
of compounds that attract females (Resink et al., 1989). In gobies, the mesorchial region of the
testes associated with the mesenteries, is hypertrophied and laden with Leydig cells that actively
secrete conjugated steroids (a variety of 5β-reduced steroids, chiefly 17-oxo-5β-androstan-3α-yl,
also known as etiocholanolone glucoronide, or ETIO-g) that attract females (Colombo, Bekvedere,
and Pilati, 1977; Colombo et al., 1980; Murphy, Stacey, and Corkum, 2001; Arbuckle et al., 2005).
Interestingly, the black goby has both territorial and sneaker male mating tactics, but only the
territorial males possess a hypertrophied mesorchial gland (Locatello, Mazzoldi, and Rasotto, 2002).
The absence of a mesorchial gland in sneaker males suggests selection for chemical crypsis (i.e.,
secondary loss of pheromone-producing tissue).
Fish that do not show obvious tissue specialization for production and release of sex pheromones
may nevertheless have an intersexual cascade of pheromonal communication that governs gonadal
maturation and spawning behavior that ensures simultaneous gamete release. For example, the
release of 17, 20β-dihydroxy-4-pregen-3-one (17, 20βP), sulfated (17, 20βP-20S) and androstenone
by pre-ovulatory female goldfish stimulate male reproductive behaviors and sperm production
(Sorensen and Stacey, 1999). While 17, 20βP is released via the gills, 17,20βP-20S is released in
pulses of urine, giving females voluntary control over its release (Sorensen et al., 1995). Ovulation
is accompanied by a 100-fold increase in prostaglandin F2α (PGF2α) (Sorensen et al., unpublished
results). PGF2α and a related metabolite 15-keto-PGF2α are released primarily with pulses of urine,
which increase in frequency when in the presence of a male, especially at the time of entering
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vegetation where oviposition occurs (Appelt and Sorensen, 2007). In other species, such as the
Mossambique tilapia, O. mossambicus, and swordtail (Xiphophorus birchmanni), it is the males that
increase the rate of urine release when in the presence of a pre-ovulatory female (Almeida et al.,
2005; Rosenthal et al., 2011). Interestingly, anosmic male tilapia did not increase rate of urination in
the presence of pre-ovulatory females indicating that the urination of males is based solely in
response to pheromones released by pre-ovulatory females (Miranda et al., 2005). Males in another
cichlid, Astatotilapia burtoni, showed a similar urinary response to visual stimuli alone, with low
rates of urination when presented with mouth-brooding (nonreceptive) females but increasing urination rate when presented with non-mouth-brooding females (Maruska and Fernald, 2012). Urine containing sex pheromones are released by O. mossambicus in contexts other than reproduction. Socially
dominant males increase concentrations of urinary sex steroids (Oliveira, Almada, and Canario, 1996)
and frequency of urine pulse release (Barata et al., 2007) in male–male social interactions.
Taken together, these studies provide evidence from disparate phylogenies for selection on context
and timing of release of behaviorally active chemical compounds by both sexes. By commonly
accepted communication theory (e.g., Bradbury and Vehrencamp, 2011), these chemical cues should
be considered signals in a co-evolved communication system, and thus, qualify as true pheromones.
7.8 Discussion: Evolution of Semiochemicals from Cues to Signals
This book on fish pheromones covers a range of semiochemicals released by conspecifics that can
be arranged across the evolutionary spectrum from cues to signals, showing an incremental transition
from basic information gathering to the elaboration of specialized receptors and mechanisms for
production and release of pheromones. The term “pheromone” was first coined by Karlson and
Lüscher (1959), as a form of chemical communication between conspecifics. Karlson and Lüscher
(1959) defined pheromone using examples from insects (social Hymenoptera, Isoptera, Lepidoptera),
sexual attractants in Crustacea, alarm pheromone [which we are now careful to call alarm cues
because senders do not benefit from the response of receivers (Ferrari, Wisenden, and Chivers, 2010;
Wisenden, 2015)] in minnows and territorial marking substances of carnivorous mammals. Wyatt
(2009, 2010, 2013) reviewed 50 years of research on pheromones across many taxa and updated the
definition: “Pheromones are molecules that are evolved signals which elicit a specific reaction, for
example, a stereotyped behavior and/or a developmental process in a conspecific.” (Wyatt, 2010).
Clearly, fish produce and respond to semiochemicals that qualify as pheromones as per Wyatt’s definition of the term. However, the majority of semiochemicals used by fishes are not pheromones by
this definition. Most fish “pheromonal” systems are in fact precommunication processes in which
receivers exploit chemical forms of public information while providing no selection on senders to
specialize in production or release of semiochemicals. Future work on fish communication should
emphasize the demonstration of evidences of specialization for detection, production, and contextspecific active release of semiochemicals. To do that, we must first acquire much more information
about the chemical nature of the compounds, often comprising mixtures of compounds, which fish
use to inform their behavioral decision-making for migration, foraging, predator avoidance, and
reproduction.
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