evolution of dynamic signaling philip stoddard & michael markham dept. biological sciences...

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.