Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes

<p>Abstract</p> <p>Background</p> <p>The vertebrate brain is composed of several interconnected, functionally distinct structures and much debate has surrounded the basic question of how these structures evolve. On the one hand, according to the 'mosaic evolution h...

Full description

Bibliographic Details
Main Authors: Kolm Niclas, Winberg Svante, Gonzalez-Voyer Alejandro
Format: Article
Language:English
Published: BMC 2009-09-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/9/238
_version_ 1818903384281841664
author Kolm Niclas
Winberg Svante
Gonzalez-Voyer Alejandro
author_facet Kolm Niclas
Winberg Svante
Gonzalez-Voyer Alejandro
author_sort Kolm Niclas
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The vertebrate brain is composed of several interconnected, functionally distinct structures and much debate has surrounded the basic question of how these structures evolve. On the one hand, according to the 'mosaic evolution hypothesis', because of the elevated metabolic cost of brain tissue, selection is expected to target specific structures mediating the cognitive abilities which are being favored. On the other hand, the 'concerted evolution hypothesis' argues that developmental constraints limit such mosaic evolution and instead the size of the entire brain varies in response to selection on any of its constituent parts. To date, analyses of these hypotheses of brain evolution have been limited to mammals and birds; excluding Actinopterygii, the basal and most diverse class of vertebrates. Using a combination of recently developed phylogenetic multivariate allometry analyses and comparative methods that can identify distinct rates of evolution, even in highly correlated traits, we studied brain structure evolution in a highly variable clade of ray-finned fishes; the Tanganyikan cichlids.</p> <p>Results</p> <p>Total brain size explained 86% of the variance in brain structure volume in cichlids, a lower proportion than what has previously been reported for mammals. Brain structures showed variation in pair-wise allometry suggesting some degree of independence in evolutionary changes in size. This result is supported by variation among structures on the strength of their loadings on the principal size axis of the allometric analysis. The rate of evolution analyses generally supported the results of the multivariate allometry analyses, showing variation among several structures in their evolutionary patterns. The olfactory bulbs and hypothalamus were found to evolve faster than other structures while the dorsal medulla presented the slowest evolutionary rate.</p> <p>Conclusion</p> <p>Our results favor a mosaic model of brain evolution, as certain structures are evolving in a modular fashion, with a small but non-negligible influence of concerted evolution in cichlid fishes. Interestingly, one of the structures presenting distinct evolutionary patterns within cichlids, the olfactory bulbs, has also been shown to evolve differently from other structures in mammals. Hence, our results for a basal vertebrate clade also point towards a conserved developmental plan for all vertebrates.</p>
first_indexed 2024-12-19T20:50:41Z
format Article
id doaj.art-13e5a51a91294c2795c0b2862fdcec21
institution Directory Open Access Journal
issn 1471-2148
language English
last_indexed 2024-12-19T20:50:41Z
publishDate 2009-09-01
publisher BMC
record_format Article
series BMC Evolutionary Biology
spelling doaj.art-13e5a51a91294c2795c0b2862fdcec212022-12-21T20:06:06ZengBMCBMC Evolutionary Biology1471-21482009-09-019123810.1186/1471-2148-9-238Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishesKolm NiclasWinberg SvanteGonzalez-Voyer Alejandro<p>Abstract</p> <p>Background</p> <p>The vertebrate brain is composed of several interconnected, functionally distinct structures and much debate has surrounded the basic question of how these structures evolve. On the one hand, according to the 'mosaic evolution hypothesis', because of the elevated metabolic cost of brain tissue, selection is expected to target specific structures mediating the cognitive abilities which are being favored. On the other hand, the 'concerted evolution hypothesis' argues that developmental constraints limit such mosaic evolution and instead the size of the entire brain varies in response to selection on any of its constituent parts. To date, analyses of these hypotheses of brain evolution have been limited to mammals and birds; excluding Actinopterygii, the basal and most diverse class of vertebrates. Using a combination of recently developed phylogenetic multivariate allometry analyses and comparative methods that can identify distinct rates of evolution, even in highly correlated traits, we studied brain structure evolution in a highly variable clade of ray-finned fishes; the Tanganyikan cichlids.</p> <p>Results</p> <p>Total brain size explained 86% of the variance in brain structure volume in cichlids, a lower proportion than what has previously been reported for mammals. Brain structures showed variation in pair-wise allometry suggesting some degree of independence in evolutionary changes in size. This result is supported by variation among structures on the strength of their loadings on the principal size axis of the allometric analysis. The rate of evolution analyses generally supported the results of the multivariate allometry analyses, showing variation among several structures in their evolutionary patterns. The olfactory bulbs and hypothalamus were found to evolve faster than other structures while the dorsal medulla presented the slowest evolutionary rate.</p> <p>Conclusion</p> <p>Our results favor a mosaic model of brain evolution, as certain structures are evolving in a modular fashion, with a small but non-negligible influence of concerted evolution in cichlid fishes. Interestingly, one of the structures presenting distinct evolutionary patterns within cichlids, the olfactory bulbs, has also been shown to evolve differently from other structures in mammals. Hence, our results for a basal vertebrate clade also point towards a conserved developmental plan for all vertebrates.</p>http://www.biomedcentral.com/1471-2148/9/238
spellingShingle Kolm Niclas
Winberg Svante
Gonzalez-Voyer Alejandro
Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
BMC Evolutionary Biology
title Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
title_full Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
title_fullStr Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
title_full_unstemmed Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
title_short Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
title_sort brain structure evolution in a basal vertebrate clade evidence from phylogenetic comparative analysis of cichlid fishes
url http://www.biomedcentral.com/1471-2148/9/238
work_keys_str_mv AT kolmniclas brainstructureevolutioninabasalvertebratecladeevidencefromphylogeneticcomparativeanalysisofcichlidfishes
AT winbergsvante brainstructureevolutioninabasalvertebratecladeevidencefromphylogeneticcomparativeanalysisofcichlidfishes
AT gonzalezvoyeralejandro brainstructureevolutioninabasalvertebratecladeevidencefromphylogeneticcomparativeanalysisofcichlidfishes