Exploring the Evolutionary Origins of the Manakin's Elaborate Courtship Dance

Key Points:

* Researchers have revealed that in manakins, small birds inhabiting Central and South America, adaptation to a frugivorous diet preceded the evolution of flamboyant courtship behaviors and vibrant plumage.

* It was discovered that manakins acquired the ability to sense the taste of sugars in fruits by repurposing their umami receptors.

* The study suggests that changes in diet, accompanied by fundamental physiological shifts in taste perception and digestion, may have spurred subsequent evolutionary changes in behavior and reproductive strategies, ultimately leading to the creation of biodiversity.

Abstract:

A research team led by Associate Professor Yasuka Toda of the School of Life Science and Technology, Tokyo University of Science (Science Tokyo), and Professor Yoshiro Ishimaru of the Department of Agricultural Chemistry, Faculty of Agriculture, Meiji University, in collaboration with Dr. Maude Baldwin, Director at the Max Planck Institute, and Associate Professor Christopher Balakrishnan of the University of East Carolina, conducted an integrated study of genomic, functional, and evolutionary analyses on manakins, small birds found in Central and South America. Their findings reveal that adaptation to a frugivorous diet preceded the evolution of elaborate courtship behaviors and vibrant plumage.

In manakins, only the males possess brightly colored plumage, exhibiting a marked sexual dimorphism compared to females. Furthermore, males display particularly complex and acrobatic courtship behaviors, including somersaults, aerial jumps, and rapid wing beats that produce sound. However, the evolutionary background of how these extreme and sophisticated behaviors originated has not been fully elucidated.

The research group performed comparative genomic analysis of five manakin species and conducted population genomics and evolutionary analyses. They discovered positive selection acting on genes such as the taste receptor T1R (Term 1) and the digestive enzyme LPH (lactase-phlorizin hydrolase). Functional analysis of the proteins produced by these genes using cultured cells revealed that manakins have acquired the ability to detect sugars with the umami receptor T1R1/T1R3. Additionally, a decrease in LPH function may prevent the formation of toxic compounds in the body when consuming unripe fruits. This suggests that manakins can efficiently utilize nutrient-rich fruits.

These physiological changes occurred earlier than the evolution of flamboyant plumage and courtship behaviors. In other words, adaptation to a frugivorous diet may have provided the foundation for strong sexual selection that followed.

This research indicates that the evolution of fundamental physiological functions, such as sensory perception (taste) and digestion, supported dietary changes, which in turn drove large-scale evolutionary changes in behavior and reproductive strategies, potentially leading to the creation of biodiversity. These findings were published in the journal Current Biology on June 10 (11:00 AM EST).

1. Lance-tailed manakin (Chiroxiphia lanceolata [scientific name], Harioce Manakin). Compared to the female (right), the male (left) has vibrant plumage. It is specialized for a frugivorous diet. Photographer: Esteban Mendez, Location: Isla Boca Brava, Panama

Background:

Sexual selection, driven by competition for mates, as exemplified by the plumage of the male peacock, is a significant factor in the evolution of diverse forms and behaviors in organisms. In birds, species known for their flamboyant plumage and courtship displays, such as manakins, birds-of-paradise, and cotingas, belong to different families but are all specialized frugivores. However, the relationship between this diet and the evolution of plumage and courtship behaviors is not well understood.

This study focused on manakins, small birds distributed in Central and South America. Many manakin species form communal courtship grounds (leks) where males engage in intense courtship competition for females. Concurrently, they are highly specialized frugivores, inhabiting tropical regions where fruits are available year-round. While the link between the utilization of nutrient-rich fruits and sexual selection has been suggested, the genetic and physiological underpinnings have not been fully clarified.

Research Findings:

This study conducted comparative genomic analysis of five manakin species, along with other birds. The results showed that in manakins, genetic diversity on the sex chromosomes (Z chromosome) is reduced compared to autosomes, indicating long-term, strong sexual selection where only a subset of males successfully reproduces. Furthermore, positive selection was detected in numerous genes related to diet, including sugar transporters and enzymes involved in metabolism and digestion, as well as taste receptors.

Functional analysis of taste receptors further revealed that manakins have acquired the ability to sense sugars using umami receptors (T1R1/T1R3), which normally cannot recognize sugars. Birds generally lack the T1R2 gene (Tas1r2), which forms the sweet taste receptor (T1R2/T1R3), and thus cannot perceive the taste of sugars. However, manakins gained the ability to detect sugars in fruits by repurposing their umami receptors as sugar receptors. This functional shift occurred early in the evolutionary history of manakins and is closely related to their adaptation to a frugivorous diet.

Detailed functional analysis of taste receptors using cultured cell systems identified 22 amino acid mutations crucial for acquiring sugar-sensing ability. Umami receptors have a structure embedded in the cell membrane, with taste substances in food primarily binding to a large exposed extracellular region. Many of the identified amino acid mutations involved in sugar sensing were concentrated in the extracellular region of T1R3 (Figure 2).

This research team has previously reported that hummingbirds, passerines, and woodpeckers that utilize nectar and fruits also possess umami receptors that have acquired sugar-sensing capabilities [References 1-3]. Interestingly, while hummingbirds, like manakins, had important amino acid mutations concentrated in the extracellular region of T1R3, in passerines, which are more closely related to manakins than hummingbirds are, the mutations were mainly concentrated in the extracellular region of T1R1 (Figure 2). These results indicate that while manakins, like other nectar-feeding birds, use umami receptors to detect the taste of sugars, this function was acquired independently through distinct amino acid mutations in each lineage.

Figure 2. Amino acid residues (colored regions) contributing to the acquisition of sugar-sensing ability. Sugar-sensing ability was acquired independently in multiple bird lineages that utilize nectar and fruits. In hummingbirds and manakins, numerous important amino acid mutations were identified in the extracellular region of T1R3, whereas in passerines, which are more closely related to manakins than hummingbirds are, important amino acid mutations were predominantly found in the extracellular region of T1R1.

Furthermore, functional analysis of digestive enzymes revealed changes in the function of lactase (LPH) (Figure 3). This enzyme is well-known in humans for breaking down lactose in milk but also plays a role in breaking down glycosides found in fruits. Some glycosides can produce toxic compounds when broken down, and unripe fruits tend to contain higher levels of these defensive substances to deter consumption before ripening. While some manakin species are known to consume unripe fruits, how they avoid toxicity has been unclear. This study suggests that manakins may excrete toxic compounds without generating them by reducing the LPH activity for breaking down glycosides.

Moreover, the acquisition of sugar taste detection and the reduced function of digestive enzymes preceded the evolution of flamboyant plumage and complex courtship behaviors (Figure 3).

This research demonstrates a link between adaptation to a frugivorous diet and sexual selection. It also suggests that the evolution of fundamental physiological functions, such as taste perception and digestion, supported dietary changes. The utilization of fruits, a high-energy resource, may have enabled single-parental care by females, consequently intensifying male reproductive competition and driving the evolution of flamboyant plumage and elaborate courtship behaviors.

Figure 3. Dietary shift and changes in digestive and taste functions in manakins. The acquisition of sugar taste detection and the reduced function of the digestive enzyme (lactase) occurred prior to the advancement of flamboyant plumage and courtship behaviors. (Modified from figures in Current Biology. Bird illustrations: Lynx Nature Books / Cornell Lab of Ornithology; N. chrysocephalum and M. vitellinus © Kristen Orr)

Societal Impact:

This research comprehensively elucidates the relationship between diet, the underlying physiological functions, and the evolution of behavior, and is expected to contribute to our understanding of the process of biodiversity creation.

Future Prospects:

The unique ecology of manakins has long attracted the interest of researchers worldwide. While studies have been conducted from various perspectives, including behavior, physiology, and morphology, this research presents a new framework connecting these aspects at the genomic level. Future expansion of such integrated approaches to other bird species and vertebrates is expected to lead to the elucidation of general principles regarding how the evolution of diet and physiological functions (such as taste and digestion) drives the evolution of behavior and reproductive strategies.

Addendum:

This research was supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS) (JP18KK0166, JP20H02941, JP22KK0079, JP23H02168, JP25H01362), the Japan Science and Technology Agency (JST) Strategic Creative Research Promotion Program (JPMJFR220C), the Lotte Foundation Research Grant, and the Meiji University International Joint Research Project Support Program.

References:

[1] Baldwin#, Toda# et al., Science 345:929-933 (2014). DOI: 10.1126/science.1255097 (#co-first author) [2] Toda et al., Science 373:226-231 (2021). DOI:10.1126/science.abf6505 [3] Cramer et al., Curr Biol 32:4270-4278 (2022). DOI: 10.1016/j.cub.2022.07.059

Glossary:

(1) Taste receptor T1R: In vertebrates, umami and sweet tastes are perceived by T1R receptors, which are G protein-coupled receptors. Mammals have three genes: T1R1, T1R2, and T1R3. The combination of T1R1 and T1R3 (T1R1/T1R3) forms the umami receptor, while the combination of T1R2 and T1R3 (T1R2/T1R3) forms the sweet taste receptor. Birds, which evolved from carnivorous dinosaurs, have lost the T1R2 gene that forms the sweet taste receptor and do not possess the sweet taste receptor T1R2/T1R3. (2) Positive selection: A phenomenon where a gene or trait confers an advantage for survival or reproduction, leading to the spread and increase of its variants within a population.

Publication Information:

Journal: Current Biology

Article Title: Genomic and physiological changes in a sexually selected and frugivorous bird radiation

Authors: Christopher N. Balakrishnan*,#, Yasuka Toda*,#, Meng-Ching Ko#, Morgan E. Wirthlin#, Robert J. Driver#, Peri E. Bolton#, Eliot T. Miller#, Daniel Mendez-Aranda#, Rebecca B. Dikow, Paul B. Frandsen, Elsie H. Shogren, Kevin F. P. Bennett, H. Luke Anderson, Madeline G. Bursell, Julia F. Cramer, Keren R. Sadanandan, Tomoya Nakagita, Marco A. Pizo, Daniel S. Caetano, Marina Anciaes, Carolina F. Ferreira, Jacob S. Berv, Kira M. Long, Haw Chuan Lim, Andre E. Moncrieff, Sarah E. Kingston, Noor D. White Carreiro, Samantha R. Friedrich, Camilo Alfonso Cuta, James B. Pease, Alexander A. Nevue, Chad Tomlinson, Aleksey Zimin, Matthew I. M. Louder, Michael S. Brewer, Rachael A. Bay, Kristen Ruegg, Thomas B. Smith, Yoshiro Ishimaru, Andreas R. Pfenning, Carolina Frankl-Vilches, Manfred Gahr, Claudio V. Mello, Rebecca T. Kimball, Edward L. Braun, John G. Blake, Lainy B. Day, T. Brandt Ryder, Ignacio T. Moore, Brent M. Horton, Barney A. Schlinger, Matthew J. Fuxjager, Wesley C. Warren, Emily H. DuVal, W. Alice Boyle, Bette A. Loiselle, Michael J. Braun, Maude W. Baldwin* (#co-first author, *co-corresponding author)

DOI: 10.1016/j.cub.2026.05.021

Researcher Profiles:

Yasuka Toda Associate Professor, Department of Life Science and Technology, School of Life Science and Technology, Tokyo University of Science Visiting Researcher, Meiji University Research Fields: Food Science, Molecular Biology

Yoshiro Ishimaru Professor, Department of Agricultural Chemistry, Faculty of Agriculture, Meiji University Research Fields: Food Science, Molecular Biology