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First published online May 19, 2008
Journal of Experimental Biology 211, 1814-1818 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015982
The adaptive evolution and processing of sensory systems |
Molecular evolution of communication signals in electric fish
Sections of Neurobiology and Integrative Biology, The University of Texas, Austin, TX 78712, USA
* Author for correspondence (e-mail: h.zakon{at}mail.utexas.edu)
Accepted 28 March 2008
Summary
Animal communication systems are subject to natural selection so the imprint of selection must reside in the genome of each species. Electric fish generate electric organ discharges (EODs) from a muscle-derived electric organ (EO) and use these fields for electrolocation and communication. Weakly electric teleosts have evolved at least twice (mormyriforms, gymnotiforms) allowing a comparison of the workings of evolution in two independently evolved sensory/motor systems. We focused on the genes for two Na+ channels, Nav1.4a and Nav1.4b, which are orthologs of the mammalian muscle-expressed Na+ channel gene Nav1.4. Both genes are expressed in muscle in non-electric fish. Nav1.4b is expressed in muscle in electric fish, but Nav1.4a expression has been lost from muscle and gained in the evolutionarily novel EO in both groups. We hypothesized that Nav1.4a might be evolving to optimize the EOD for different sensory environments and the generation of species-specific communication signals. We obtained the sequence for Nav1.4a from non-electric, mormyriform and gymnotiform species, estimated a phylogenetic tree, and determined rates of evolution. We observed elevated rates of evolution in this gene in both groups coincident with the loss of Nav1.4a from muscle and its compartmentalization in EO. We found amino acid substitutions at sites known to be critical for channel inactivation; analyses suggest that these changes are likely to be the result of positive selection. We suggest that the diversity of EOD waveforms in both groups of electric fish is correlated with accelerations in the rate of evolution of the Nav1.4a Na+ channel gene due to changes in selection pressure on the gene once it was solely expressed in the EO.
Key words: sodium channels, molecular evolution, communication, electric fish, electric organ, fish
Introduction
Neuroethology abounds with examples of animals' sensory systems shaped by
natural selection for optimal encoding of sensory information from their
environments or communication signals from conspecifics. Visual systems may be
optimized for night vision, specific colors or color contrast, or detection of
movement (Land, 1993
;
Warrant et al., 2004;
Kern et al., 2005). Auditory
systems may be specialized for high frequencies, low frequencies, specific
frequency bands, or specific combinations of harmonics or temporal patterns
(Kössel and Russell,
1995; Feng et al.,
2006). Olfactory systems are similarly specialized
(Rouquier et al., 2000;
Niimura and Nei, 2003;
Nozawa and Nei, 2007).
However, the functioning and evolution of sensory systems is also
intimately tied to the functioning and evolution of motor systems in two ways.
First, when acquiring information from the world around them many animals are
moving through their environments. An animal's motor systems must be tuned so
that the rate of information flow generated by its movement through the world
matches or at least does not exceed the information-encoding rate of its
sensors (Snyder et al., 2007).
For example, dusk- or night-active insects, whose retinas integrate slowly,
fly more slowly than day-active insects
(Warrant et al., 2004).
Second, animals must detect conspecific communication signals. Thus, each
species' sensory systems have evolved to detect the signal generated by their
motor systems (Gilbert and Strausfeld,
1991; Land, 1993).
In situations where rapid speciation is occurring, there must be rapid
co-evolution of the sensory and motor systems for species-specific signals
(Mendelson and Shaw, 2005;
Arnegard et al., 2006). The
most precise matching of motor output and sensory tuning occurs in animals
such as dolphins and bats that navigate in the ultrasonic range, and electric
fish that emit and detect their own electric fields.
All of these examples raise the question as to how on a molecular level
these sensory systems evolved their species-specific properties and how these
co-evolved with each species' motor systems. Most sensory/motor systems are
under complex multigenic control precluding the easy identification of
candidate genes (Hoy et al.,
1977). Our deepest understanding of this process comes from cases
of molecules specifically and obviously expressed in sensory receptors such as
opsins (Terai et al., 2002) or
olfactory receptors (Rouquier et al.,
2000; Niimura and Nei,
2003; Nozawa and Nei,
2007). Electric fish have a number of attributes that make them
good model systems for studying these questions.
Electric fish as models for molecular evolution
Electric organs (EOs) have evolved at least six times in teleost and
elasmobranch fish. The EOs of some groups generate strong discharges to stun
prey or predators (torpenid rays, uranoscopid teleosts, malapterurid catfish).
The EOs of others are seldom discharged and their function is poorly
understood (Rajidae, synodontid catfish). However, the use of EOs and
electrosensory systems for sophisticated communication (electrocommunication)
and for the detection and identification of nearby objects (electrolocation)
has evolved independently in teleosts at least twice – the gymnotiforms
of South America and the mormyriforms of Africa. This allows us to compare the
workings of evolution in two independently evolved sensory/motor systems
(Bullock et al., 2005). Their
sensory receptors, EOs, and central sensory processing and motor control areas
are remarkably similar in a striking case of parallel evolution. Electric fish
are, therefore, good model organisms for investigating whether parallel
evolution has also occurred on the molecular level.
Electric fish lend themselves to a molecular evolutionary analysis in that electric signals are already in the currency of the nervous system: electricity. Because of this, electric signals are easily understood and analyzed in terms of the biophysics of ion currents and associated with a manageable number of candidate genes (mainly encoding Na+ and K+ channels) whose expression can be localized to sensory and motor structures.
Electric fish are excellent animals for studying the coordinated evolution
of sensory and motor processes. Electric fish generate EO discharges (EODs)
from a muscle-derived EO and sense these fields with special sensory receptors
called electroreceptors, presumably derived from the same embryonic source as
lateral line hair cells (Bullock et al.,
2005). Electric fish detect nearby objects by sensing how those
objects perturb their own EODs in a process called electrolocation. EOD
waveforms are species specific, usually sexually dimorphic, and are often
individually distinct (Stoddard et al.,
2006), and electric fish communicate with conspecifics by
detecting each other's EODs. Furthermore, weakly electric fish are preyed on
by electric eels in South America (electric eels are gymnotiforms) and
electroreceptor-bearing catfish on both continents, and electric signals have
evolved to minimize detection by these predators
(Hanika and Kramer, 1999;
Stoddard, 1999). Thus, EOD
waveforms and the sensory capabilities of electroreceptors have been shaped by
the needs of electrolocation, communication and predator avoidance.
Electric fish show a number of presumably adaptive specializations. Two distinct discharge patterns occur, independently evolved in both groups: pulse- and wave-type patterns. Pulse fish emit EOD pulses, often with a complex multi-phasic structure, at irregular intervals. They vary the repetition rate of the EOD as needed, discharging at high rates when active and low rates when resting. Wave-type species discharge in a specific frequency band; males, females and juveniles may each discharge within a portion of the species bandwidth, and each fish may furthermore have its own `personal' frequency (many species of electric fish are capable of shifting their individual frequency to a new value if they are `jammed' by another fish with a similar frequency). Wave-type EOD waveforms are usually monophasic pulses of a duration roughly equal to the interpulse duration, thereby forming a sine wave-like pattern. Wave-type fish discharge constantly whether they are active or inactive.
Electric fish show a diversity of EOD waveforms. Some species produce long
duration pulses (20 ms) whereas others generate extremely brief discharges
(
200 µs; Fig. 1). This
is a hundredfold difference in EOD pulse duration. Indeed, ultra-brief
discharges have evolved in both groups of electric fish
(Bennnet, 1971). The briefer
the discharge the broader the power spectrum of the signal; broad power
spectra are beneficial for detecting a wider range of complex impedences from
objects in the environment (von der Emde
and Ringer, 1992). Some wave-type gymnotiforms discharge at low
frequencies (50 Hz) and others at very high frequencies (>1 kHz).
Presumably, sampling at high frequencies gives fish better temporal resolution
of their world. Generating such brief pulses or operating at high frequencies
may be possible because electric fish are `ion channel specialists'. That is,
they have specialized in the evolution and regulation of ion channels as a
means to generate species-specific signals [the anatomical structure of the EO
varies greatly among species and also plays a dominant role in shaping the EOD
(Hopkins, 1999)].
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Voltage clamp analysis of the ion currents in the electrocytes, the cells
of the EO, show that the EOD pulse is mainly shaped by Na+ currents
(Shenkel and Sigworth, 1991;
Ferrari et al., 1995). We
therefore focused our molecular evolutionary analysis on Na+
channel genes. When we undertook this work it was known that mammals possess
10 Na+ channel genes but there was no information on the number of
Na+ channel genes in fish, despite the fact that the first
Na+ channel gene cloned was from the EO of the electric eel, a
gymnotiform (Noda et al.,
1984). Therefore, we cloned Na+ channel genes from
representative species of both groups of weakly electric fish, a catfish and a
lamprey (as an outgroup for gnathostomes), and assembled additional
Na+ channel genes by cloning or from genome databases for zebrafish
and pufferfish. We found that teleosts have seven to eight Na+
channel genes. Phylogenetic studies indicate that the common ancestor of
teleosts and tetrapods had four Na+ channel genes and that these
duplicated at the origin of teleosts
(Lopreato et al., 2001;
Novak et al., 2006),
presumably as part of a teleost-specific genome-wide duplication (i.e. ploidy)
event (Amores et al., 1998;
Jaillon et al., 2004;
Crow et al., 2006).
Since EOs derive from muscle, we were especially interested in the
orthologs of the mammalian muscle Na+ channel gene Nav1.4
(Nav1.4=scn4a). We found that fish possess two duplicate
copies: Nav1.4a and Nav1.4b. Not surprisingly, analysis of
muscle mRNA by PCR showed that both genes are expressed in the muscles of
non-electric fish (Venkatesh et al.,
2005; Zakon et al.,
2006; Novak et al.,
2006). At this level of resolution, however, we do not know
whether both genes are expressed redundantly in every muscle fiber or whether
each gene is separately expressed in a subset of muscle fibers (slow
vs fast, hypaxial vs epaxial, etc). This can be tested by
in situ hybridization or single cell PCR.
The situation is different in electric fish. Nav1.4b is also
expressed in muscle in electric fish and, in addition, may be expressed in the
EO in some species. However, Nav1.4a expression has been lost in
muscle and gained in the evolutionarily novel EO in both groups of electric
fish (Zakon et al., 2006) (M.
Arnegard, D.Z., Y.L. and H.H.Z., unpublished observations).
A notable exception to this pattern is the weakly electric fish the brown
ghost, Apternotus leptorhynchus. This species (and the large
radiation of other apteronotid species) has a myogenically derived larval EO
that is retained only for the first few weeks of larval life during which time
its EOD frequency is only a few hundred hertz
(Kirschbaum, 1977). As
maturation continues its EOD frequency increases to 750–1000 Hz or, in
some apteronotid species, up to 1600 Hz
(Kramer et al., 1980). As the
myogenic larval EO degenerates, the axons of the motorneurons that innervated
it are altered and become the new EO
(Pappas et al., 1975). In this
way, speed and synchronization are most efficiently maintained by electrotonic
coupling from the brain down to the motorneuron and the elimination of the
single obligate chemical synapse (neuroelectrocyte junction) in the pathway.
Because the EO of mature apteronotids is not from muscle we believe that
neither Nav1.4a nor Nav1.4b, but some other neurally
expressed Na+ channel gene(s), must be responsible for generating a
rapid EOD frequency in apteronotids. Intracellular recordings from the axons
of neurogenic electrocytes show that they are capable of discharging at or
over 1000 Hz (Schaefer and Zakon,
1996). PCR or in situ hybridization analyses of the
motorneurons and of the larval EO will provide the final identity of the
Na+ channels in the adult and larval EOs.
The fact that Nav1.4a has twice lost its expression from muscle
and gained it in the novel environment of the EO is potentially informative as
to possible constraints on the evolution of Nav1.4a. Indeed, in
zebrafish, a non-electrogenic teleost, Nav1.4a is expressed in fewer
tissues than Nav1.4b (Novak et
al., 2006). Thus, it may be that fewer tissues would have been
affected by the loss of expression of Nav1.4a than Nav1.4b.
We do not know what molecular events account for altered expression of
Nav1.4a in electric fish, but analysis of regulatory regions in these
genes compared with the regulatory regions in related non-electric fish will
probably shed light on this.
Na+ channel genes are normally under strong negative selection
as evidenced by the large catalog of channelopathies (diseases attributed to
mutations in ion channels) (Wei et al.,
1999; Bendahhou et al.,
2002; Splawski et al.,
2002; Tan et al.,
2003; Tian et al.,
2004; Wang et al.,
2004; Berkovic et al.,
2004). We reasoned that in both lineages of electric fish
Nav1.4a would be freed from many selective constraints associated
with muscle expression as electrocytes are not contractile and mutations in
Nav1.4a would have no effect on a fish's motility. Furthermore, it
seemed likely that Nav1.4a is evolving under a new set of selection
pressures to optimize the EOD in different sensory environments or for the
generation of species-specific communication signals. This would be evident by
an increase in the number of non-synonymous (nucleotide substitutions that
change the amino acid) over synonymous (or `silent' substitutions, nucleotide
substitutions that do not change the amino acid) substitutions per codon.
We tested the hypotheses that: (1) Nav1.4a has evolved at a higher rate in electric than non-electric fish; (2) changes in the rate of evolution of Nav1.4a in electric fish occur following its loss of expression from muscle and gain of expression in the EO; (3) amino acid changes in the channel will be evident in regions of the channel involved in voltage-dependent gating and, specifically, inactivation (the closure of the channel despite maintained depolarization) since the distinguishing feature of EODs is that they may vary in duration.
We obtained the sequence for Nav1.4a from six non-electric, one
mormyriform and four gymnotiform species, constructed a phylogenetic tree and
estimated the number of non-synonymous vs synonymous changes per
codon in each lineage (Zakon et al.,
2006) (Fig. 2). We
found that the single mormyrid and all the gymnotiform electric fish except
for Apteronotus showed elevated ratios of non-synonymous/synonymous
substitutions in Nav1.4a compared with the same gene in non-electric
teleosts. This is consistent with our hypothesis that loss of Nav1.4a
expression from muscle was permissive for elevated rates of amino acid
substitutions. We have since confirmed these results with a larger data set
from both electric lineages (M. Arnegard, D.J.Z., Y.L. and H.H.Z., unpublished
observations). Furthermore, in order to confirm that the elevation in the
non-synonomous/synonymous ratio was not due to an increase in this ratio in
all genes of these species, we performed the same analysis on
Nav1.4b, which is still expressed in the muscle in both groups of
weakly electric fish, and found that there was no difference in the rates of
evolution in this gene between electric and non-electric fish (M. Arnegard,
D.J.Z., Y.L. and H.H.Z., unpublished observations). Likelihood-based analyses
(PAML) support the contention that these changes are the result of positive
selection. In these analyses, there was a difference in the distribution of
changes at the codon level in Nav1.4a of some of the electric fish
that were not observed in Nav1.4a of non-electric species (or
Apteronotus leptorhynchus). As implemented, these tests identified
branches in the tree (i.e. taxa) that showed elevated rates of non-synonymous
substitutions, but they did not have the power to identify specific sites at
which positive selection might have occurred.
|
;
Kellenberger et al., 1997;
Popa et al., 2004). Despite
the persistence of conserved amino acids in these regions across 500
million years of evolution (tunicates–vertebrates), we noted changes in
key amino acids in these sites in both groups of weakly electric fish. In the
single mormyrid that we studied, we noted amino acid substitutions at two key
residues in the domain III–IV loop `inactivation ball'
(Fig. 3D) whereas in the
gymnotiforms we noted substitutions in the domain III S4–S5 linker
(Fig. 3C), which is one of the
binding partners of the inactivation ball. We also noted amino acid
substitutions in the S4–S5 linker in domain II
(Fig. 3B) in both groups. In
agreement with our suggestion that amino acid mutations that occur in these
regions will be selected against because they might cause pathology, we
indicate in the figure mutations that have been noted in the human clinical
literature and associated with muscular, cardiac or neurological disease
(Wei et al., 1999;
Bendahhou et al., 2002;
Splawski et al., 2002;
Tan et al., 2003;
Tian et al., 2004;
Wang et al., 2004;
Berkovic et al., 2004). These
mutations flank (Fig. 3B,C,E)
or occur at the same (Fig. 3C)
amino acids at which we witness evolutionary changes in electric fish
channels.
We conclude that the diversity of EOD waveforms in both groups of electric
fish is correlated with accelerations in the rate of evolution of the
Nav1.4a Na+ channel gene. The placement of some of these
amino acid substitutions in key regions involved in inactivation further
suggests that these substitutions will affect the rates of Na+
current inactivation (Zakon et al.,
2006).
Future directions
Pinpointing likely amino acid changes that underlie the evolution of Na+ channel genes is a big step in understanding the evolution of electric signaling in electric fish. However, understanding how these substitutions actually alter the biophysical properties of the Na+ currents can only be approached by site-directed mutagenesis and expression of channels.
A second intriguing direction is investigating the molecular events that led to the loss of Nav1.4a expression from muscle and, even more interesting, how the genes that are expressed in the EO come to recognize the novel phenotype of the EO. This analysis can be commenced by cloning and sequencing upstream regulatory regions of Nav1.4a in a number of species in which the gene is still expressed in muscle (apteronotids and non-electric outgroups) and those in which it is lost (most electric fish) to determine whether there are any radical alterations or losses of particular transcription factor binding sites.
Apteronotid electric fish probably use a different Na+ channel gene since Nav1.4a is not expressed in the CNS (Y.L. and H.H.Z., unpublished observations). Identification of the Na+ channel genes that are expressed in the apteronotid pacemaker or electromotorneurons by PCR would be a profitable first step. Once candidate genes are identified, a similar analysis to the one described here could be performed.
In an analogous manner to that in which EOs have evolved from muscle in fish, specialized muscles for the generation of species-specific acoustic communication signals have evolved multiple times in teleosts. These muscles generate sounds by the rapid compression and relaxation of the swimbladder at rates exceeding 100 Hz. It would be interesting to test whether a similar pattern of compartmentalization and specialization of either Nav1.4a or Nav1.4b has occurred in these specialized sound-producing muscles.
Na+ channels have associated subunits called β subunits that modify the biophysical properties of the Na+ channel proper. In addition, the repolarization of the action potential is through K+ channels. It will be intriguing to determine whether other ion channels evolved in parallel with Na+ channels.
Acknowledgments
The authors thank the NIH (H.Z., Y.L) and NSF (D.H., D.Z.) for funding, and The Company of Biologists for hosting a wonderful meeting.
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