Abstract
The mammalian neocortex has undergone repeated selection for increases and decreases in size and complexity, often over relatively short evolutionary time. But because probing developmental mechanisms across many species is experimentally unfeasible, it is unknown whether convergent morphologies in distantly related species are regulated by conserved developmental programs. In this work, we have taken advantage of the abundance of available mammalian genomes to find evidence of selection on genomic regions putatively regulating neurogenesis in large- versus small-brained species. Using published fetal human RNA-seq data, we show that the gene-neighborhood (i.e., microsynteny) of long intergenic non-coding RNAs (lincRNAs) implicated in cortical development is differentially conserved in large-brained species, lending support to the hypothesis that lincRNAs regulating neurogenesis are selectively lost in small-brained species. We provide evidence that this is not a phenomenon attributable to lincRNA expressed in all tissue types and is therefore likely to represent an adaptive function in the evolution of neurogenesis. A strong correlation between transcription factor-adjacency and lincRNA sequence conservation reinforces this conclusion.
Highlights
We used previously published RNA-seq data (Series GSE38805) collected from the ventricular zone (VZ), inner subventricular zone (ISVZ), outer subventricular zone (OSVZ), and cortical plate (CP) of human fetal neocortex at gestation week (GW)13–16 [22] and employed the lincRNA discovery pipeline outlined by [30] to identify 187 lincRNA differentially expressed during human neocortical neurogenesis (Fig 1A–1D, S1 Table)
We identified 187 lincRNAs differentially expressed in a germinal zone or the cortical plate (CP) of the embryonic human neocortex (Fig 1A–1D, S1 Table)
We found that all low-gyrencephaly index (GI) species fell below and all high-GI species above phylogenetic expectations (Fig 2B), with two exceptions: the marmoset, a near-lissencephalic primate that is hypothesized to have recently evolved from a gyrencephalic ancestor and may still be in the process of purging unneeded neurodevelopmental lincRNAs [42]; and the manatee, a large-brained (382g), albeit lissencephalic species [43]
Summary
Development of the neocortex, like most aspects of development [3], retains a much stricter pattern across species, involving a conserved arsenal of progenitor-types. These major progenitor-types—apical radial glia (aRG) and basal radial glia (bRG), as well as apical and basal intermediate progenitors (IPs)—are putatively present in all mammals [4, 5, 6, 7]. In those mammals with larger, convoluted neocortices (i.e., gyrencephalic species), a heterogeneity of bRGs is observed [8], and an increased proliferative potential in basally dividing progenitors is important for cortical size and folding
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