10/6/2011 The Authors Brain Evolution Triggers Increased Dr. Bruce A. Carlson Diversification of Electric Fishes • Principal Investigator • Professor, Department of Biology @ Washington Bruce A. Carlson, Saad M. Hasan, University in St. Louis Michael Hollmann, Derek B. Miller, Luke • Cornell University, Ph.D. in J. Harmon, and Matthew E. Arnegard J Harmon and Matthew E Arnegard Neurobiology & Behavior Neurobiology & Behavior Journal: Science 332 , 583 ‐ 586 Dr. Matthew E. Arnegard Published: April 29, 2011 • NIH Post ‐ Doctoral Edward Kim Research Fellow October 4, 2011 • Cornell University, Ph.D. in Neurobiology & Behavior The Authors The Authors Derek B. Miller Dr. Luke Harmon Saad M. Hasan • Assistant Professor, Department of • Undergraduate student • Student at Cornell Weill Biology @ University of Idaho at Washington University Medical College • Washington University in St. Louis, in St. Louis, studying • B.S. at Washington Ph.D. in Evolution, Ecology, and Biology & Physics gy y University in St Louis University in St. Louis Population Biology Population Biology Dr. Michael Hollmann • Professor, Department of Chemistry and Biochemistry @ Ruhr University Bochum Science Electric Fish ( Mormyridae ) • Published by the American Association for the Advancement of Science • Impact factor: 31 36 • Impact factor: 31.36 • First publication: 1880 1
10/6/2011 Mormyridae and the evolution of Diversity of Signal waveforms temporal coding • Brief Overview • Relevant Brain Regions • How changes in the brain enable temporal coding – Impact of temporal coding Impact of temporal coding – Mechanism of temporal coding • How the ability drives signal diversification and speciation Mormyridae and the evolution of Electric signaling is key temporal coding • Brief Overview • Signals are critical for species recognition • Relevant Brain Regions • Signals evolve faster than other factors like • How changes in the brain enable temporal coding body shape, size, or trophic ecology. • Mormyridae are the ideal model system for – Impact of temporal coding Mormyridae are the ideal model system for Impact of temporal coding relating brain evolution to diversification. Why? – Mechanism of temporal coding • How the ability drives signal diversification and speciation Electrical signaling is key Electroreceptors • Signals are critical for species recognition • Signals evolve faster than other factors like body shape, size, or trophic ecology. • Mormyridae are the ideal model system for Mormyridae are the ideal model system for relating brain evolution to diversification. Why? – Easy to study: a specific sensory pathway exists exclusively for electric communication analysis 2
10/6/2011 Mormyridae and the evolution of Electroreceptors temporal coding • The timing of knollenorgan response on different • Brief Overview parts of the body gives information about the • Relevant Brain Regions stimulus. • How changes in the brain enable temporal coding • The projections eventually reach a midbrain region – Impact of temporal coding Impact of temporal coding called the exterolateral nucleus (EL). – Mechanism of temporal coding • How the ability drives signal diversification and speciation The Exterolateral nucleus (EL) Brain evolution and diversification? • Pathway: the • A comparative analysis knollenorgan (KO) of EL anatomy was projects to the nucleus performed, through of the electrosensory standard procedures of lateral line lobe (nELL), obtaining brain slices which projects to the EL • 26 species Difference in ELp/ELa & EL expression, The EL has two forms in Mormyridae within subfamilies Mormyrinae and Petrocephalinae • The EL was identified using topology (spatial relations to other brain regions, regardless of shape/size). • In some cases, the EL was a single, small unit with no subdivisions. In others, it was divided into the anterior and posterior regions (ELa and ELp, respectively) 3
10/6/2011 Cytb data suggests a phylogenetic Two exceptions separation between EL and ELa/ELp • Mormyrinae is a monophyletic group, and all but ELa / ELp one have ELa / ELp subdivisions (“Clade A”) – Exception: Mormyrinae myomyrus • Petrocephalinae is a monophyletic group, and all but one show no EL subdivisions – Exception: Petrocephalus microphthalmus . New discovery in this study. EL • But there is a problem… Parsimony Parsimony • Maximum parsimony ‐ • Maximum parsimony ‐ when facing competing evolutionary hypotheses, choose the one with the fewest assumptions. – in this case, the least evolutionary change Parsimony Parsimony • Maximum parsimony ‐ when facing competing • Maximum parsimony ‐ when facing competing evolutionary hypotheses, choose the one with the evolutionary hypotheses, choose the one with the fewest assumptions. fewest assumptions. – in this case, the least evolutionary change – in this case, the least evolutionary change • So, either EL is the ancestral state and ELa/ELp is • So, either EL is the ancestral state and ELa/ELp is derived, or ELa/ELp is ancestral and EL is derived. derived, or ELa/ELp is ancestral and EL is derived. • Which is more parsimonious? • Which is more parsimonious? – Phylogenetic analysis does not give us an answer. 4
10/6/2011 Mormyridae and the evolution of Gymnarchus settles the debate temporal coding • Brief Overview • New data on the • Relevant Brain Regions brain structure of – Exterolateral nucleus Gymnarchus , the – Phylogenetic divide between EL & ELa/ELp y g p sister taxon to sister taxon to • How changes in the brain enable temporal coding the Mormyridae, – Impact of temporal coding reveals an unseparated EL, – Mechanism of temporal coding demonstrating • How the ability drives signal diversification and that EL is the speciation ancestral state So why does the presence of an EL EL division & receptor distribution division matter? • Results: Clade A & P. • Hypothesis: EL anatomy is responsible for different microphthalamus show broad distribution of distribution of receptors. receptors • All other Petrocephalinae • Two patterns of receptor organization Two patterns of receptor organization show clusters on the head show clusters on the head – Broad distribution throughout body • Mormyrinae Myomyrus is – Discrete clusters on head intermediate (one cluster on head, sparse distribution thru body) • Testing the hypothesis • Conclusion: ELa/ELp is – Method: mapping knollenorgans of species responsible for broad distribution Distribution of receptors Distribution of receptors • How does a broad or clustered distribution of • How does a broad or clustered distribution of receptors affect temporal coding? receptors affect temporal coding? – Recall: The EL analyzes electric signals by comparing response times of knollenorgans on different parts of th b d the body – So, the broad distribution of KOs should help with signal discrimination 5
10/6/2011 Playback experiment Playback experiment • Method: Fired 10 bursts (each • Results burst = 10 pulses). The 9 th – Clade A & P. microphthalamus exhibited dishabituation burst was phase ‐ shifted, and changes in behavior from the (and partial recovery of response) 8 th to 9 th recording was recorded. – Petrocephalinae did not show a dishabituation • • Normal response to a Normal response to a conspecific is either 1) increase in electric discharge, • Conclusion: the evolution of ELa/ELp led to or 2) pause in electric output • physical changes that improves signal Deviations from the normal response (increasing elec discrimination ability discharge rate, or pausing for longer) indicate dishabituation and thus discrimination of the changed nature of the signal Arnegard et al., 2006 Mormyridae and the evolution of Temporal Coding: Mechanism temporal coding • Knollenorgans respond • Brief Overview differently with the onset • Relevant Brain Regions of current from one side • How changes in the brain enable temporal coding of the body to the other. – Impact of temporal coding Impact of temporal coding – The first would respond Th fi t ld d – Mechanism of temporal coding with the normal polarity (receiving the EOD • How the ability drives signal diversification and stimulus), while the speciation opposite side would respond with the reverse polarity (responding to an inverted EOD stimulus) M. Xu ‐ Friedman & C.D. Hopkins, 1999 Temporal Coding: Mechanism Temporal Coding: Mechanism • The ELa contains large • Recall: the KO projects cells and small cells. to NELL (nucleus of the • NELL contacts a large cell, electrosensory lateral and after a delay, some line lobe) which small cells • The ELa large cells form Th EL l ll f projects to ELa and an inhibitory synapse on medialis ventralis (MV) the small cells. • ELa is specialized for • The result is that a small cell receives an inhibitory time keeping input from the large cell, – Heavy myelination and a delayed excitatory – Thick axons input from a NELL cell. M. Xu ‐ Friedman & C.D. Hopkins, 1999 M. Xu ‐ Friedman & C.D. Hopkins, 1999 6
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