Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

Abstract
Data availability
Article and author information
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Abstract

Brain region size generally scales allometrically with brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes (Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis. Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual major brain regions independent of brain size, suggesting that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

Data availability

Brain measurement data is located in Supplementary File 1. Brain mass data is located in Supplementary File 2. All analysis code and phylogenetic trees are available in Dryad. The raw micro-computed tomography scans are too large to post (multiple TBs), but are available upon request. To request raw otophysan and/or osteoglossiform scans, contact the corresponding author. We ask that those who want access to the scan data send us an external hard drive, which we will upload all the data to and then return.

The following data sets were generated

1. Schumacher EL
2. Carlson B
(2022) Data from: Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes
Dryad Digital Repository, doi:10.5061/dryad.7d7wm37w5.

https://dx.doi.org/10.5061/dryad.7d7wm37w5

The following previously published data sets were used

1. Tsuboi M
2. van der Bijl W
3. Kopperud BT
4. Erritzoe J
5. Voje KL
6. Kotrschal A
7. et al
(2018) Data from: Brain mass and body mass datasets and phylogenies linked to brain-body allometry and the encephalization of birds and mammals.
Figshare, doi:10.6084/m9.figshare.6803276.v1.

https://doi.org/10.6084/m9.figshare.6803276.v1
1. Tsuboi M
(2021) Data from: Exceptionally Steep Brain-Body Evolutionary Allometry Underlies the Unique Encephalization of Osteoglossiformes
Brain Behav Evol, Supplementary Material, doi:10.1159/000519067.

https://doi.org/10.1159/000519067
(2018) Data from: Extreme Enlargement of the Cerebellum in a Clade of Teleost Fishes that Evolved a Novel Active Sensory System
Curr Biol, doi:10.1016/j.cub.2018.10.038.

https://doi.org/10.1016/j.cub.2018.10.038

Article and author information

Author details

Erika L Schumacher

Department of Biology, Washington University in St. Louis, St. Louis, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2492-1117
Bruce A Carlson

Department of Biology, Washington University in St. Louis, St. Louis, United States

For correspondence
carlson.bruce@wustl.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2151-0443

Funding

National Science Foundation (IOS-1755071)

Bruce A Carlson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The methods in this study are consistent with euthanasia guidelines by the American Veterinary Medical Association and have been approved by the Animal Care and Use Committee at Washington University in St. Louis (Protocol ID 19-0974).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.