Correlated Evolution of Acrobatic Display and Both Neural and Somatic Phenotypic Traits in Manakins (Pipridae)

Abstract

Brightly colored manakin (Aves: Pipridae) males are known for performing acrobatic displays punctuated by non-vocal sounds (sonations) in order to attract dull colored females. The complexity of the display sequence and assortment of display elements involved (e.g., sonations, acrobatic maneuvers, and cooperative performances) varies considerably across manakin species. Species-specific display elements coevolve with display-distinct specializations of the neuroanatomical, muscular, endocrine, cardiovascular, and skeletal systems in the handful of species studied. Conducting a broader comparative study, we previously found positive associations between display complexity and both brain mass and body mass across eight manakin genera, indicating selection for neural and somatic expansion to accommodate display elaboration. Whether this gross morphological variation is due to overall brain and body mass expansion (concerted evolution) versus size increases in only functionally relevant brain regions and growth of particular body ("somatic") features (mosaic evolution) remains to be explored. Here, we test the hypothesis that cross-species variation in male brain mass and body mass is driven by mosaic evolution. We predicted positive associations between display complexity and variation in the volume of the cerebellum and sensorimotor arcopallium, brain regions which have roles in sensorimotor processes, and learning and performance of precisely timed and sequenced thoughts and movements, respectively. In contrast, we predicted no associations between the volume of a limbic arcopallial nucleus or a visual thalamic nucleus and display complexity as these regions have no-specific functional relationship to display behavior. For somatic features, we predicted that the relationship between body mass and complexity would not include contributions of tarsus length based on a recent study suggesting selection on tarsus length is less labile than body mass. We tested our hypotheses in males from 12 manakin species and a closely related flycatcher. Our analyses support mosaic evolution of neural and somatic features functionally relevant to display and indicate that sexual selection for acrobatic complexity increases the capacity for procedural learning via cerebellar enlargement and may decrease maneuverability via increases in tarsus length.