Evolution of dynamic signaling
Philip Stoddard & Michael Markham
Dept. Biological Sciences
Florida International University
Dr. Michael Markham
Other contributors from the lab
Dr. Cheryl Franchina
Justin Tackney
Our Sponsors
Susan Allee
Vicky Salazar
Anya Goldina
National Institutes of Health
NIGMS MBRS, NINDS, NIMH, NHLBI
Evolution of a new communication system
Evolution of a new communication system
lust
anger
fear
ennui
hunger
sex
size
condition
endurance
strength
What evolutionary changes allows a signal to
communicate state, motivation, & emotion?
Part 1
Constraints and historic response to sensory drive
Classic model
restraint
Sexual
Selection
Predation &
Physiological costs
elaboration
Sexual Selection
Cost gradient model
showy or
costly
cryptic or
low cost
Multiplicative costs of natural selection
(e.g., predator density or energetic cost)
Sexual Selection
Cost gradient model
Predator density
Photos by K. Hughes, K. McGhee, and C. Gibson
Sexual Selection
Dynamic signaling can escape constraints
showy or
costly
dynamic
cryptic or
low cost
Multiplicative costs of natural selection
(e.g., predator density or energetic cost)
Fixed signals
Dynamic signals
• structural colors & pigments
• expensive ornaments
• weapons
• active displays
• transient signals
(calls & songs)
Dynamics:
• on / off
• variable magnitude
• variable spectrum
Convey genetic or
developmental quality,
and condition.
Can also convey
transient states of
motivation or emotion.
Why most fish make electricity
1. Seeing in the dark
(they are nocturnal)
r
c
Why most fish make electricity
1.
2.
Seeing in the dark
Communicating in the dark
Electric courtship songs
Electric Organ Discharge = EOD
EOD fixed by physiology of excitable
membranes in the electrocyte.
electric field
electrocyte
EOD waveform
Development of electrocytes
Myocytes fuse in development to form electrocytes
Shape changes, 2nd phase appears
Fusing
Myocytes
Larval
Electrocytes
Mature
Electrocytes
C. Franchina & P. Stoddard
The EOD MACHINE
Recording calibrated electric signals around the clock
Recording EODs in free-swimming fish
www
Stoddard, Markham, Salazar 2003 J. Exp. Biol
Signal costs: EOD energetics
Pharmacological partitioning of the energy budget
Salazar & Stoddard subm
O2 consumption ≈ energetic cost
x 10-4
6
R2 = 0.790
p = 0.001
µL O2 / EOD
x 10-3
7
female
male
4
6
5
4
2
0
R2 = 0.9900
p = 0.0001
3
0
0.1
0.2
2
1
0
5
10
15
20
Power (mV2) EOD-1
0
Salazar & Stoddard subm
Male EOD energy expense (VO2)
is condition-dependent
Partial regression
weight adjusted for length
0.2
0.1
Residual
VO2 EOD
R2=0.75
p=0.008
0
-0.1
-0.2
-4
-2
0
2
Residual weight
4
Salazar & Stoddard subm
The classic sensory dilemma:
Ampullary electroreceptor system is
used by females in mate choice
& by predators for finding prey
Active Electrolocation
- listening to own EOD
mV/cm
100
10
1
tuberous
0.1
ampullary
0.01
0.1
1
10
100
1,000
Physiology adapted from Dunning 1973
Passive Electrolocation
Shumway & Zelick 1988
10,000 Hz
Tuberous
Ampullary
Yes
No
Yes
Yes
Yes
Yes
Low frequency (ampullary) content of synthetic
courtship signals is critical for spawning
no spawning
elicits spawning
based on Hagedorn (1986)
Problem predators - catfish & electric eel
electroreceptive
electrogenic too
phylogeny after Lauder & Leim 1983
~12 million years before Star Trek
electric fish evolved active cloaking to
conceal their signals from predators
“In several science fiction universes, a cloaking
device is an advanced stealth system which
causes a spaceship or individual to be invisible
and extremely difficult to detect with normal
sensors. However, the idea of a cloaking device
could be extended to any object and is not
restricted simply to spacecraft.”
Wikipedia
2 ways to cloak an EOD
compensatory
pulse
0v
0v
DC offset
current
EOD symmetry suppresses low frequency energy
EOD Waveforms
1 ms
Biphasic 1st phase
EOD
alone
Power Spectra
Does electric cloaking really work?
Ask a predator
Playback to Sparky the electric eel
an electroreceptive predator
EOD Waveforms
Power Spectra
1 ms
Biphasic 1st phase
EOD
alone
Approach
0.25 0.67 (p=0.01, Fisher exact test)
Frequency
Stoddard 1999 Nature
Cloaking evolved 4X in gymnotiforms
Phylogeny from Albert et al. 1998
Brachyhypopomus pinnicaudatus
waveform symmetry develops for cloaking
then is lost in males
17 days
30 days
50 days
110 days
sexual
maturity
1 ms
Spectral consequences of asymmetry
Sexy signals make happy catfish
Thursday evening
Friday morning
p = 0.067
Attractive to catfish
NOT attractive to catfish
dB
dB
0
0
Hypopotamyrus
angsorii
-20
-40
0
102
-40
104 Hz
0
Hypopotamyrus
sp. nov.
0
102
-40
104
Marcusenius
macrolepidotus
- male
Cyphomyrus
discorhynchus
0
102
104
0
102
Marcusenius
macrolepidotus
- female
-20
-40
104
0
0
102
104
0
Marcusenius
macrolepidotus
- male
-20
1 ms
104 Hz
0
-20
-40
102
-20
0
-40
0
0
-20
-40
Petrocephalus
catostoma
-20
0
102
-20
-40
104
“eat me”
Petrocephalus
casteinaui
0
102
104
1 ms
adapted from Hanika & Kramer 2000
Part 2: dynamic control of the EOD
Cloaking &
energy conservation
Enhancement
Cryptic
electrolocation
Social
signaling
Only these
taxa modulate
their EOD
waveforms
Markham, Goldina, Stoddard in prep
Consensus phylogeny from Albert et al. 1998
Dynamic regulation of the EOD
% incr.
2500%
2000%
1500%
QuickTime™ and a
Animation decompressor
are needed to see this picture.
1000%
500%
0%
Male B. pinnicaudatus
cloaks his signal by day
and uncloaks it at night
EOD waveform
EOD spectrum
Stoddard 2002 Adv Study Behav
TauP2, a useful metric
amplitude
duration of
2nd phase
time constant = tauP2
Male circadian rhythms are stronger
(males reveal more, cloak less)
males
tauP2
females
days
Stoddard, Markham, Salazar, Allee in press.
Enhancement of male EOD depends on his relative status
Fish added to tank:
tauP2
smaller EOD male,
strong enhancement
0.1 ms
male w/ larger EOD,
no enhancement
24 h
Salazar & Stoddard in prep
EOD enhanced in minutes by social stress
tau-P2 (ms)
0.55
0.45
0.35
08:00
0.30
2nd
fish
2nd
removed
fish
placed
in
tube
0.25
0.20
15:00 08:00
12:00
12:00
time of day
Stoddard, Markham, Salazar 2003 J. Exp. Biol
Handling stress enhances the EOD
tauP2
Markham & Stoddard 2005 J Neurosci
What evolutionary change connected
the EOD to so much information?
• Body condition
• Circadian state
• Relative social status
• Social stress
• Physiological stress
At night all fish are gray
Our hypothesis:
Dynamic EOD control adapted from
the skin pigmentation control system.
Cebra-Thomas 2001
Melanocortin peptide hormones
(-MSH & ACTH)
darken melanophores by
dispersing melanosomes.
Logan et al. 2006
B. pinnicaudatus electrocytes express mRNA
of melanocortin receptors (MCRs)
580 base pair
product
electrocytes
brain
Touchdown gradient RT-PCR with
degenerate primers for MCR family
Tackney & Stoddard unpubl
1000x bootstrap of nearest-neighbor joining tree
of all published melanocortin receptor sequences.
Cloned products indicated by dots.
MC5R
MC3R
MC4R
MC1R
MC2R
Tackney & Stoddard unpubl
MCR5
amino acid sequences
Sequence homology > 80%
Tackney & Stoddard unpubl
Melanocortins do it
baseline
ACTH injected
Markham, Goldina, Stoddard in prep
Consensus phylogeny from Albert et al. 1998
MC CR
?
?
Markham, Goldina, Stoddard in prep
Melanocortins work directly on electrocytes
baseline
ACTH
EOD from a single cell in a dish
Markham & Stoddard 2005 J Neurosci
Androgen potentiates melanocortin action
before
5-DHT
implant
baseline
ACTH injected
after
5-DHT
implant
baseline
ACTH injected
1 ms
amplitudes rescaled to match P1
Allee, Markham, Stoddard in prep.
The rest of the pathway
(for another talk)
Serotonin (5-HT)
5HT1AR & 5HT2AR
CRF & TRH
[CRFxR]
ACTH & MSH
MCR5
Adenylyl cyclase
cAMP
Protein Kinase A
Na+, K+ channels
hypothalamus
pituitary
periphery
(electrocytes)
MSH melanocortins are body fat signals
in vertebrates - work with leptin & NPY
Lipolysis 
MC3R
MSH & MSH
MC4R
Appetite 
MC5R
EOD 
Neuroendocrine cascade of
dynamic EOD enhancement & cloaking
Social
environment
Brain
GnRH
LH
Serotonin
CRF / TSH
ACTH / -MSH
Testes
Androgens
Electrocytes
Melanocortin receptor 5
Cyclic AMP (cAMP)
Protein kinase A (PKA)
Phosphorylatable ion channels
Components shared with the vertebrate
skin pigmentation control system
Social
environment
Brain
GnRH
LH
Serotonin
CRF / TSH
ACTH / -MSH
Testes
Androgens
Electrocytes
Melanocortin receptor 5
Cyclic AMP (cAMP)
Protein kinase A (PKA)
Phosphorylatable ion channels
Components shared with the mammalian preputial
aggression/sex pheromone system
Social
environment
Brain
GnRH
LH
Serotonin
CRF / TSH
ACTH / -MSH
Testes
Androgens
Electrocytes
Melanocortin receptor 5
Cyclic AMP (cAMP)
Protein kinase A (PKA)
Phosphorylatable ion channels
1. What happened:
Sexual Selection
Sensory conflicts were partially resolved
by dynamic regulation of fixed-trait signals
showy or
costly
dynamic
cryptic or
low cost
Multiplicative costs of natural selection
(e.g., predator density or energetic cost)
2. Favored hypothesis of how
dynamic communication evolved:
Expression of ancient MC5R gene allows EOD
to communicate state, motivation, & emotion
Postdoc and graduate study opportunities available.