Abstract
Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.
Highlights
Characterizing the molecular basis for the evolution of convergent traits may help us to understand the genetics of adaptation
Examples of convergent genetic changes contributing to convergent traits include cis-regulatory or protein coding mutations in: i) a pigmentation gene that generates similar but independently evolved wing spots in multiple fruit fly species [4]; ii) a homeobox transcription factor that leads to pelvic reduction in independent lineages of both stickleback fish and mammals [5]; iii) a sodium channel gene that was important for the evolution of electric organs in independent lineages of electric fish [6]; and iv) the melanocortin 1 receptor gene responsible for coat and skin color variation across vertebrates [2]
In contrast to the rest of the brain, we found that the vast majority (.95%) of cells labeled in RA, LMAN, and dorsal medial (DM) were double-labeled for dusp1 and egr1 (Fig. 3C,E)
Summary
Characterizing the molecular basis for the evolution of convergent traits may help us to understand the genetics of adaptation. Examples of convergent genetic changes contributing to convergent traits include cis-regulatory or protein coding mutations in: i) a pigmentation gene that generates similar but independently evolved wing spots in multiple fruit fly species [4]; ii) a homeobox transcription factor that leads to pelvic reduction in independent lineages of both stickleback fish and mammals [5]; iii) a sodium channel gene that was important for the evolution of electric organs in independent lineages of electric fish [6]; and iv) the melanocortin 1 receptor gene responsible for coat and skin color variation across vertebrates [2] All of these examples are traits involving a convergent phenotype that is visible in the organism. It is generally agreed the both songbirds and parrots are distantly related to hummingbirds
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