Adult pallium transcriptomes surprise in not reflecting predicted homologies across diverse chicken and mouse pallial sectors

Abstract

The thorniest problem in comparative neurobiology is the identification of the particular brain region of birds and reptiles that corresponds to the mammalian neocortex [Butler AB, Reiner A, Karten HJ (2011) Ann N Y Acad Sci 1225:14-27; Wang Y, Brzozowska-Prechtl A, Karten HJ (2010) Proc Natl Acad Sci USA 107(28):12676-12681]. We explored which genes are actively transcribed in the regions of controversial ancestry in a representative bird (chicken) and mammal (mouse) at adult stages. We conducted four analyses comparing the expression patterns of their 5,130 most highly expressed one-to-one orthologous genes that considered global patterns of expression specificity, strong gene markers, and coexpression networks. Our study demonstrates transcriptomic divergence, plausible convergence, and, in two exceptional cases, conservation between specialized avian and mammalian telencephalic regions. This large-scale study potentially resolves the complex relationship between developmental homology and functional characteristics on the molecular level and settles long-standing evolutionary debates.

Keywords: Wulst; brain evolution; cerebral cortex; dorsal ventricular ridge; equivalent circuit hypothesis.

Fig. 1.

Studied regions and little conservation of gene coexpression between avian and mammalian brains. Brain regions involved in the evolutionary debate of neocortex homology studied in mouse (A) and chicken (B) were dissected from serial sections in the anteroposterior axis; the claustrum (Cl, dashed lines) is located in more anterior sections of mammalian brains, and the arcopallium (A) is located in more posterior sections of avian brains. The avian dorsolateral corticoid area is shown in SI Appendix, Fig. S8. (C) Topological dissimilarity dendrogram and coexpressed mouse modules. Gene pairs that branch from one another lower on this dissimilarity dendrogram have more similar expression patterns across the dissected samples than other pairs. A color band corresponds to a group of genes sharing a similar expression pattern across samples; thus, larger bands reflect more genes that share a pattern. (D) Topological dissimilarity dendrogram and coexpressed chicken modules. (E) Relative positions in the chicken dendrogram (represented in B) of one-to-one orthologs of genes in the mouse clustering (represented in A). (F) Relative positions in the mouse dendrogram (represented in A) of one-to-one orthologs of genes in the chicken clustering (represented in B). A to F in mouse, cortical layers; Ag, basolateral amygdala; dCx, dorsal cerebral cortex; E, endopiriform complex; H, hyperpallium; Hp, hippocampus; lCx, lateral cerebral cortex; M, mesopallium; N, nidopallium; S, striatum.

Fig. 2.

Conserved striatal and hippocampal gene coexpression modules in chicken and mouse. (A) Expression correlations between genes in two striatal chicken gene coexpression modules and one striatal gene coexpression module in mouse with significant overlap between the two species (chicken striatal module 1 overlapping with Bonferroni-corrected P = 8.7 × 10⁻²¹, chicken striatal module 2 overlapping with Bonferroni-corrected P = 1.4 × 10⁻⁴; both hypergeometric tests). (B) RNA in situ hybridization (ISH) of conserved markers of chicken striatum. (C) RNA-ISH of conserved markers of mouse striatum. (D) Expression correlations between genes in significantly overlapping chicken and mouse hippocampal gene coexpression modules (Bonferroni-corrected P = 3.6 × 10⁻³, hypergeometric test). (E) RNA-ISH of conserved markers of chicken hippocampus. (F) RNA-ISH of conserved markers of mouse hippocampus. CDL, corticoid dorsolateral area. (Scale bars: black, 500 μm; red, 200 μm.)

Fig. 3.

Convergent gene coexpression modules marking chicken nidopallium and mouse layer IV. (A) Expression correlations between genes in significantly overlapping gene coexpression modules expressed in chicken nidopallium and mouse layer IV (Bonferroni-corrected P = 4.6 × 10⁻³, hypergeometric test). (B) RNA-ISH of convergent nidopallium markers. (C) RNA-ISH of convergent layer IV markers. (Scale bars: black, 500 μm; gray, 200 μm.) Cx, neocortex; en, entopallium; LIV, neocortical layer IV. (Scale bars: black, 500 μm; red, 200 μm.)