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Artificial mosaic brain evolution of relative telencephalon size improves cognitive performance in the guppy (Poecilia reticulata)
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0001-5592-8963
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The telencephalon is a brain region believed to have played an essential role during cognitive evolution in vertebrates. However, till now, all the evidence on the evolutionary association between telencephalon size and cognition stems from comparative studies. To investigate the potential evolutionary association between cognitive abilities and telencephalon size experimentally, we used male guppies artificially selected for large and small telencephalon relative to the rest of the brain. We tested a functionally important aspect of executive cognitive ability, inhibitory control, in a detour task and found that males with larger telencephalon outperformed males with smaller telencephalon. Theyshowed faster improvement in performance during detour training and weremore successful in reaching the food reward without touching the transparent barrier. Together, our findings provide the first experimental evidence showing that evolutionary enlargements of relative telencephalon size confer cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.

Keywords [en]
Relative telencephalon size, inhibitory control, detour task, male guppies, fish
National Category
Zoology
Research subject
Zoology; Ethology
Identifiers
URN: urn:nbn:se:su:diva-186330OAI: oai:DiVA.org:su-186330DiVA, id: diva2:1484807
Funder
Swedish Research Council, 2016-03435Available from: 2020-10-30 Created: 2020-10-30 Last updated: 2022-02-25Bibliographically approved
In thesis
1. Brain morphology and behaviour in the guppy (Poecilia reticulata): Effects of plasticity and mosaic brain evolution
Open this publication in new window or tab >>Brain morphology and behaviour in the guppy (Poecilia reticulata): Effects of plasticity and mosaic brain evolution
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding how brains have evolved and subsequently culminated in the huge variation in brain morphology among contemporary vertebrate species has fascinated researchers for many decades. It has been recognized that brain morphology is both genetically and environmentally determined. Adaptations to ecological challenges, for one, has been proposed to be a major force in brain diversification processes. Considering the large energetic costs of neural tissue, it is believed that brain evolution is a highly complex process, involving a delicate balance between the corresponding costs and benefits. 

Using the guppy (Poecilia reticulata) as the model organism, I first examined the conditions under which diversity in brain morphology is generated. This was done by investigating factors known to exert an influence on brain plasticity, namely environmental and cognitive effects (Paper I). Existing studies generally indicate that the provision of environmental enrichment lead to the enlargement of specific brain structures. While plastic alterations in brain morphology was found to respond to environmental complexity in my study, successful performance in two cognitive tasks did not produce any significant changes. 

I next assessed the feasibility of the mosaic brain evolution hypothesis by artificially selecting for an increase and decrease in the relative size of the telencephalon (Paper II). Telencephalon size was shown to respond rapidly to divergent selection pressures, with no substantial changes in any of the other brain regions. A comparison with wild fish revealed that fish from the unselected control treatment had telencephalon sizes most similar to that of wild populations, whereas both up-selected and down-selected fish had considerably larger and smaller telencephalon, respectively. 

I tested fish from the artificial selection lines in a test battery to determine if known differences in telencephalon size affects boldness (Paper III). Individuals were subjected to an emergence test, an open field test and a novel object test. I found no differences in boldness levels across selection treatments, but distinct sex differences were noted whereby males were more active and bolder. 

The cognitive benefits associated with a larger telencephalon were examined in males in a test of self-control (Paper IV). Guppies from the up-selected lines attained a steeper learning curve and made more correct detours compared to their down-selected conspecifics. 

In conclusion, I provide experimental evidence for the mosaic brain evolution hypothesis by showing that a specific brain region (telencephalon) can evolve rapidly and independently under directed selection. Future tests on other cognitive benefits as well as implicated costs, together with underlying neuronal changes would help to further unravel the factors governing brain evolution.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2020. p. 38
Keywords
brain plasticity, cognition, reversal learning, spatial learning, directed selection, mosaic brain, heritability, brain morphology, boldness, relative telencephalon size, inhibitory control, detour task, Poecilia reticulata
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-186357 (URN)978-91-7911-348-3 (ISBN)978-91-7911-349-0 (ISBN)
Public defence
2020-12-17, online via Zoom, public link is available at the department web site, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2020-11-24 Created: 2020-11-02 Last updated: 2022-02-25Bibliographically approved

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Triki, ZegniFong, StephanieKolm, Niclas

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