期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：14
DOI：10.1073/pnas.2119671119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
The process by which new complex traits evolve has been a persistent conundrum throughout the history of evolutionary inquiry. How multiple physiological changes at the organism level and genetic changes at the molecular level combine is still unclear for many traits. Here, we studied the displays of manakins, who beat their wings together at nearly twice the speed of other songbirds to produce a loud “snap” that attracts mates. We simultaneously analyzed evolution of gene expression levels and gene sequences to identify key genes related to muscle contractions and tissue regeneration after stress. Our results show how innovative behavioral traits evolve as a layered process where recent molecular shifts build on ancestral genetic evolutionary changes.
Identifying the molecular process of complex trait evolution is a core goal of biology. However, pinpointing the specific context and timing of trait-associated changes within the molecular evolutionary history of an organism remains an elusive goal. We study this topic by exploring the molecular basis of elaborate courtship evolution, which represents an extraordinary example of trait innovation. Within the behaviorally diverse radiation of Central and South American manakin birds, species from two separate lineages beat their wings together using specialized “superfast” muscles to generate a “snap” that helps attract mates. Here, we develop an empirical approach to analyze phylogenetic lineage-specific shifts in gene expression in the key snap-performing muscle and then integrate these findings with comparative transcriptomic sequence analysis. We find that rapid wing displays are associated with changes to a wide range of molecular processes that underlie extreme muscle performance, including changes to calcium trafficking, myocyte homeostasis and metabolism, and hormone action. We furthermore show that these changes occur gradually in a layered manner across the species history, wherein which ancestral genetic changes to many of these molecular systems are built upon by later species-specific shifts that likely finalized the process of display performance adaptation. Our study demonstrates the potential for combining phylogenetic modeling of tissue-specific gene expression shifts with phylogenetic analysis of lineage-specific sequence changes to reveal holistic evolutionary histories of complex traits.
