Research ArticleEVOLUTIONARY BIOLOGY

Divergence in problem-solving skills is associated with differential expression of glutamate receptors in wild finches

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Science Advances  14 Mar 2018:
Vol. 4, no. 3, eaao6369
DOI: 10.1126/sciadv.aao6369
  • Fig. 1 Study species.

    (A) Portion of the phylogenetic tree of the Thraupidae family that includes T. bicolor and L. barbadensis (38). (B) In the wild, L. barbadensis is bold, opportunistic, and highly innovative, whereas (C) T. bicolor is shy, conservative, and noninnovative. (D) Number of trials needed to complete the obstacle removal problem. L. barbadensis completed the task in a mean of 4.4 ± 1.09 trials, but none of the tested T. bicolor solved it within the 15 allocated trials. (E) The number of trials to reach the success criterion in the detour reaching task was lower in L. barbadensis (15.7 ± 2.3 trials, n = 29) than in T. bicolor (26.4 ± 4.6 trials, n = 15; *PMann-Whitney = 0.0143). Means ± SEM. Photo credit: S. Ducatez, McGill University.

  • Fig. 2 RNA-seq analysis of L. barbadensis and T. bicolor transcriptomes.

    (A) Schematic view of the avian brain (16), with the regions that were examined in this study colored in green. (B) PCA of gene expression pattern per species and per region. Individual blue (L. barbadensis) and red (T. bicolor) circles include the mean of the reads from all individuals for a given species/region. The orange outline designates the regions that form the associative pallium (mesopallium and nidopallium, including NCL). (C) Gene ontology (GO) clustering analysis of differentially expressed genes, using, separately, the whole data set of differentially expressed genes, the genes that are up-regulated in L. barbadensis (L.b.), or the genes that are up-regulated in T. bicolor (T.b.). The three clusters with the highest enrichment scores are shown (all P < 0.05 except myelination P = 0.0517). Cell. comm., cellular communication. (D) Considering only the genes that are characterized by synaptic (Synap) and neuronal (Neuro) GO terms, the number of genes that are up-regulated in L. barbadensis is higher than the number of genes that are up-regulated in T. bicolor in the associative pallium. **P < 0.01. (E) Using the same subset of genes, the number of genes that are up-regulated in L. barbadensis were compared to the number of genes that are up-regulated in T. bicolor in each of the regions. L. barbadensis had more up-regulated genes in the NCL. **P < 0.01. The total number of differentially expressed genes is significantly higher in the associative pallium than in the three other regions. ***P < 0.001. (F) Two significant constructed network modules: “Synapse” and “Adult Behavior.” See fig. S7 for all other modules. Both have a positive r value, indicating that the mean expression in the modules is higher in L. barbadensis compared to T. bicolor. Hippo, hippocampus; IH, intercalated hyperpallium; MD, dorsal mesopallium; MV, ventral mesopallium; Ento, entopallium; LSt, lateral striatum; MSt, medial striatum; B, basorostralis; LMD, lamina mesopallium dorsale; LMI, lamina mesopallium intermediate; LMV, lamina mesopallium ventrale; LPS, lamina pallio-subpallialis; Meso, mesopallium; Nido, nidopallium; Arco, arcopallium.

  • Fig. 3 Glutamate receptor expression analysis.

    (A) RNA-seq data (variance stabilizing transformation of reads) of all glutamate receptors. P values were obtained by differential expression analysis. (B) Representative autoradiography images of glutamate receptor in situ hybridizations (ISH). (C) Quantification of the signal obtained by in situ hybridization for all assessed glutamate receptors. Significantly different expression is indicated by colored bars. Means ± SEM. *P < 0.05, **P < 0.01, ***P < 0.001.

  • Fig. 4 GRIN2A and GRIN2B expression across all brain regions.

    (A) In situ hybridizations of GRIN2A and GRIN2B mRNA with their mean GRIN2B/GRIN2A ratios below, calculated with the quantifications of individual receptor expression in each region. (B) Immunohistochemistry (IHC) targeting proteins with GRIN2A- and GRIN2B-specific antibodies, with their mean GRIN2B/GRIN2A ratios below, calculated with the quantifications of individual receptor expression in each region. (C) Heatmaps of mean expression (vsd-transformed reads) for GRIN2A and GRIN2B from RNA-seq data. Bottom: Mean ratios calculated with individual receptors. Means ± SEM. *P < 0.05, **P < 0.01, ***P < 0.001. Scale bars, 500 μm.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/3/eaao6369/DC1

    Supplementary Materials and Methods

    fig. S1. Behavioral tasks.

    fig. S2. Problem solving and shaping.

    fig. S3. Risk-taking behavior and discrimination learning.

    fig. S4. Residual brain mass of our two species versus other thraupids.

    fig. S5. Cluster analysis of gene expression per region and MA plots showing the distribution in the two species of fold change in all genes as a function of expression, for each analyzed brain region.

    fig. S6. Proportion of differentially expressed genes and absolute number of up-regulated genes for specific GO terms.

    fig. S7. Network dendrogram and modules following weighted correlation network analysis.

    fig. S8. GRIN2A and GRIN2B expression across all brain regions.

    table S1. Linear model outputs for all behavioral variables.

    table S2. Mean expression of each glutamate receptor in each region, using in situ hybridization and RNA-seq data.

    References (4046)

  • Supplementary Materials

    This PDF file includes:

    • Supplementary Materials and Methods
    • fig. S1. Behavioral tasks.
    • fig. S2. Problem solving and shaping.
    • fig. S3. Risk-taking behavior and discrimination learning.
    • fig. S4. Residual brain mass of our two species versus other thraupids.
    • fig. S5. Cluster analysis of gene expression per region and MA plots showing the distribution in the two species of fold change in all genes as a function of expression, for each analyzed brain region.
    • fig. S6. Proportion of differentially expressed genes and absolute number of up-regulated genes for specific GO terms.
    • fig. S7. Network dendrogram and modules following weighted correlation network analysis.
    • fig. S8. GRIN2A and GRIN2B expression across all brain regions.
    • table S1. Linear model outputs for all behavioral variables.
    • table S2. Mean expression of each glutamate receptor in each region, using in situ hybridization and RNA-seq data.
    • References (40–46)

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