evolution of dynamic signaling philip stoddard & michael markham dept. biological sciences...
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Evolution of dynamic signaling
Philip Stoddard & Michael MarkhamDept. Biological Sciences
Florida International University
Dr. Michael Markham
Other contributors from the lab
Dr. Cheryl FranchinaDr. Cheryl Franchina Susan AlleeSusan Allee
Our Sponsors National Institutes of HealthNational Institutes of Health
NIGMS MBRS, NINDS, NIMH, NHLBINIGMS MBRS, NINDS, NIMH, NHLBI
Justin TackneyJustin Tackney Anya GoldinaAnya Goldina
Vicky SalazarVicky Salazar
Evolution of a new communication system
Evolution of a new communication system
lustangerfearennuihunger
What evolutionary changes allows a signal to communicate state, motivation, & emotion?
sexsizeconditionendurancestrength
Part 1
Constraints and historic response to sensory drive
Classic model
restraint
elaboration
Predation &Predation &Physiological costsPhysiological costsSexualSexual
SelectionSelection
Sex
ual S
elec
tion
Multiplicative costs of natural selection(e.g., predator density or energetic cost)
Cost gradient model
showy orcostly
cryptic orlow cost
comprom
ise
Sex
ual S
elec
tion
Predator density
Cost gradient model
Photos by K. Hughes, K. McGhee, and C. Gibson
Comprom
ise line
Sex
ual S
elec
tion
Multiplicative costs of natural selection(e.g., predator density or energetic cost)
Dynamic signaling can escape constraints
showy orcostly
cryptic orlow cost
dynamic
comprom
ise
Fixed signals
• structural colors & pigments• expensive ornaments• weapons
Dynamic signals
• active displays • transient signals
(calls & songs)
Dynamics:• on / off• variable magnitude• variable spectrum
Can also convey transient states of motivation or emotion.
Convey genetic or developmental quality,and condition.
cr
Why most fish make electricity
1. Seeing in the dark (they are nocturnal)
Why most fish make electricity
Electric courtship songs
1. Seeing in the dark
2. Communicating in the dark
Electric Organ Discharge = EODEOD fixed by physiology of excitable
membranes in the electrocyte.
electrocyte EOD waveformelectric field
Development of electrocytes Myocytes fuse in development to form electrocytesShape changes, 2nd phase appears
C. Franchina & P. Stoddard
FusingMyocytes
LarvalElectrocytes
MatureElectrocytes
The EOD MACHINEThe EOD MACHINERecording calibrated electric signals around the clockRecording calibrated electric signals around the clock
Recording EODs in free-swimming fishRecording EODs in free-swimming fish
Stoddard, Markham, Salazar 2003 J. Exp. BiolStoddard, Markham, Salazar 2003 J. Exp. Biol
www
Salazar & Stoddard subm
Signal costs: EOD energetics
Pharmacological partitioning of the energy budget
0 0 . 1 0 . 2
0
2
4
6
x 1 0 - 4
m a le
f e m a le
0 5 1 0 1 5 2 00
1
2
3
4
5
6
7
x 1 0 - 3
R 2 = 0 . 9 9 0 0
p = 0 . 0 0 0 1
R 2 = 0 .7 9 0
p = 0 .0 0 1
P o w e r ( m V 2 ) E O D - 1
µ L O2
/ E O D
O2 consumption ≈ energetic cost
Salazar & Stoddard subm
Male EOD energy expense (VO2) is condition-dependent
-4 -2 0 2 4-0.2
-0.1
0
0.1
0.2
Partial regressionweight adjusted for length
ResidualVO2 EOD
Residual weight
R2=0.75p=0.008
Salazar & Stoddard subm
Physiology adapted from Dunning 1973 Shumway & Zelick 1988
0.1 1 10 100 1,000 10,000 Hz0.01
0.1
1
10
100mV/cm
tuberous
ampullary
Passive Electrolocation - including predatory eavesdroppers
Active Electrolocation - listening to own EOD
The classic sensory dilemma:Ampullary electroreceptor system isused by females in mate choice & by predators for finding prey
TuberousAmpullary
YesNo
YesYes
YesYes
Low frequency (ampullary) content of synthetic courtship signals is critical for spawning
based on Hagedorn (1986)
no spawning
elicits spawning
Problem predators - catfish & electric eel
electrogenic too
electroreceptive
phylogeny after Lauder & Leim 1983
~12 million years before Star Trek~12 million years before Star Trekelectric fish evolved active cloaking to electric fish evolved active cloaking to
conceal their signals from predatorsconceal their signals from predators
““In several science fiction universes, a cloaking In several science fiction universes, a cloaking device is an advanced stealth system which device is an advanced stealth system which causes a spaceship or individual to be invisible causes a spaceship or individual to be invisible and extremely difficult to detect with normal and extremely difficult to detect with normal sensors. However, the idea of a cloaking device sensors. However, the idea of a cloaking device could be extended to any object and is not could be extended to any object and is not restricted simply to spacecraft.”restricted simply to spacecraft.”
WikipediaWikipedia
compensatorypulse
2 ways to cloak an EOD
DC offsetcurrent
0 v
0 v
Power SpectraEOD Waveforms
EOD symmetry suppresses low frequency energy
BiphasicEOD
1st phasealone
1 ms
Ask a predator
Does electric cloaking really work?
Power SpectraEOD Waveforms
Playback to Sparky the electric eel an electroreceptive predator
ApproachFrequency
BiphasicEOD
1st phasealone
1 ms
0.25 0.67 (p=0.01, Fisher exact test)Stoddard 1999 Nature
Phylogeny from Albert et al. 1998
Cloaking evolved 4X in gymnotiforms
Brachyhypopomus pinnicaudatusBrachyhypopomus pinnicaudatus waveform symmetry develops for cloaking waveform symmetry develops for cloaking
then is lost in malesthen is lost in males
1 ms1 ms
17 days17 days
30 days30 days
50 days50 days
110 days110 days
sexualsexualmaturitymaturity
Spectral consequences of asymmetry
Sexy signals make happy catfish
Thursday evening Friday morning
p = 0.067
Attractive to catfish NOT attractive to catfish
adapted from Hanika & Kramer 2000
Marcuseniusmacrolepidotus- male
0
-20
-400 102 104
0
-20
-400 102 104
Marcuseniusmacrolepidotus- male
1 ms
0
-20
-40
dB
0 102 104Hz
Hypopotamyrusangsorii
0
-20
-400 102 104
Hypopotamyrussp. nov.
0
-20
-40
dB
0 102 104Hz
Petrocephaluscatostoma
Cyphomyrusdiscorhynchus
Marcuseniusmacrolepidotus- female
Petrocephaluscasteinaui
0
-20
-400 102 104
0
-20
-400 102 104
0
-20
-400 102 104
1 ms
“eat me”
Part 2: dynamic control of the EOD
Social signaling
Cloaking & Cloaking & energy conservationenergy conservation
Cryptic electrolocation
EnhancementEnhancement
Only these taxa modulate their EOD waveforms
Markham, Goldina, Stoddard in prepConsensus phylogeny from Albert et al. 1998
Dynamic regulation of the EOD
0%
500%
1000%
2000%
1500%
2500%% incr.
Oh cursed Bill Gates and his sorryexcuse for an operating system
Male B. pinnicaudatus cloaks his signal by day and uncloaks it at night
EOD waveform EOD spectrum
Stoddard 2002 Adv Study Behav
amplitude
duration of 2nd phase
time constant = tauP2
TauP2, a useful metric
Male circadian rhythms are stronger (males reveal more, cloak less)
Stoddard, Markham, Salazar, Allee in press.
males
females
days
tauP2
Enhancement of male EOD depends on his relative status
smaller EOD male,strong enhancement
male w/ larger EOD,no enhancement
0.1 ms
Salazar & Stoddard in prep
tauP2
Fish added to tank:
24 h
12:00 15:000.35
0.45
0.55
08:00
EOD enhanced in minutes by social stress
tau-P2 (ms)
time of day
2ndfish
placedin
tube
2ndfishremoved
Stoddard, Markham, Salazar 2003 J. Exp. Biol
Handling stress enhances the EOD
Markham & Stoddard 2005 J NeurosciMarkham & Stoddard 2005 J Neurosci
tauP2
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.
Logan et al. 2006
Cebra-Thomas 2001
Melanocortin peptide hormones (-MSH & ACTH)darken melanophores by dispersing melanosomes.
B. pinnicaudatus electrocytes express mRNA of melanocortin receptors (MCRs)
Touchdown gradient RT-PCR with degenerate primers for MCR family
Tackney & Stoddard unpubl
electrocytes brain
580 base pairproduct
1000x bootstrap of nearest-neighbor joining tree of all published melanocortin receptor sequences.
Cloned products indicated by dots.
Tackney & Stoddard unpubl
MC5R MC3R MC4R MC1R MC2R
MCR5 amino acid sequences
Tackney & Stoddard unpubl
Sequence homology > 80%
baselineACTH injected
Markham, Goldina, Stoddard in prepConsensus phylogeny from Albert et al. 1998
Melanocortins do it
Markham, Goldina, Stoddard in prep
MCMC
? ?
CRCR
Melanocortins work directly on electrocytes
EOD from a single cell in a dish
Markham & Stoddard 2005 J Neurosci
baselineACTH
Androgen potentiates melanocortin action
1 ms
baseline
ACTH injected
after5-DHT
implant
ACTH injected
baseline
before5-DHT
implant
amplitudes rescaled to match P1
Allee, Markham, Stoddard in prep.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 signalsin vertebrates - work with leptin & NPY
MC5R EOD
MSH & MSHMSH & MSH MC4R Appetite
Lipolysis MC3R
Neuroendocrine cascade of dynamic EOD enhancement & cloaking
Social environment Brain
SerotoninGnRH CRF / TSH
LH ACTH / -MSH
Brain Serotonin
GnRH CRF / TSH LH ACTH / -MSH
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
TestesAndrogensTestes
Androgens
Components shared with the vertebrate skin pigmentation control system
Social environment Brain
SerotoninGnRH CRF / TSH
LH ACTH / -MSH
Brain Serotonin
GnRH CRF / TSH LH ACTH / -MSH
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
TestesAndrogensTestes
Androgens
Components shared with the mammalian preputial aggression/sex pheromone system
Social environment Brain
SerotoninGnRH CRF / TSH
LH ACTH / -MSH
Brain Serotonin
GnRH CRF / TSH LH ACTH / -MSH
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
ElectrocytesMelanocortin receptor 5
Cyclic AMP (cAMP)Protein kinase A (PKA)
Phosphorylatable ion channels
TestesAndrogensTestes
Androgens
Sex
ual S
elec
tion
Multiplicative costs of natural selection(e.g., predator density or energetic cost)
1. What happened:Sensory conflicts were partially resolvedby dynamic regulation of fixed-trait signals
showy orcostly
cryptic orlow cost
dynamic
comprom
ise
2. Favored hypothesis of how dynamic communication evolved:
Expression of ancient MC5R gene allows EODto communicate state, motivation, & emotion
Postdoc and graduate study opportunities available.