Systems biology as a framework to understand the physiological and endocrine bases of behavior and its evolution-From concepts to a case study in birds

Matthew J Fuxjager; T Brandt Ryder; Nicole M Moody; Camilo Alfonso; Christopher N Balakrishnan; Julia Barske; Mariane Bosholn; W Alice Boyle; Edward L Braun; Ioana Chiver; Roslyn Dakin; Lainy B Day; Robert Driver; Leonida Fusani; Brent M Horton; Rebecca T Kimball; Sara Lipshutz; Claudio V Mello; Eliot T Miller; Michael S Webster; Morgan Wirthlin; Roy Wollman; Ignacio T Moore; Barney A Schlinger

doi:10.1016/j.yhbeh.2023.105340

Systems biology as a framework to understand the physiological and endocrine bases of behavior and its evolution-From concepts to a case study in birds

Horm Behav. 2023 May:151:105340. doi: 10.1016/j.yhbeh.2023.105340. Epub 2023 Mar 16.

Authors

Matthew J Fuxjager¹, T Brandt Ryder², Nicole M Moody³, Camilo Alfonso⁴, Christopher N Balakrishnan⁵, Julia Barske⁶, Mariane Bosholn⁷, W Alice Boyle⁸, Edward L Braun⁹, Ioana Chiver¹⁰, Roslyn Dakin², Lainy B Day¹¹, Robert Driver⁵, Leonida Fusani¹², Brent M Horton¹³, Rebecca T Kimball⁹, Sara Lipshutz¹⁴, Claudio V Mello¹⁵, Eliot T Miller¹⁶, Michael S Webster¹⁷, Morgan Wirthlin¹⁸, Roy Wollman¹⁹, Ignacio T Moore⁴, Barney A Schlinger²⁰

Affiliations

¹ Department of Ecology, Evolution, and Organismal Biology, Brown University, Providence, RI 02906, USA. Electronic address: matthew_fuxjager@brown.edu.
² Migratory Bird Center, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20013, USA.
³ Department of Ecology, Evolution, and Organismal Biology, Brown University, Providence, RI 02906, USA.
⁴ Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24060, USA.
⁵ Department of Biology, East Carolina University, Greenville, NC 27858, USA.
⁶ Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.
⁷ Animal Behavior Lab, Ecology Department, National Institute for Amazon Research, Manaus, Amazonas, Brazil.
⁸ Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
⁹ Department of Biology, University of Florida, Gainesville, FL 32611, USA.
¹⁰ GIGA Neurosciences, University of Liège, Liege, Belgium.
¹¹ Department of Biology, University of Mississippi, University, MS 38677, USA.
¹² Department of Behavioral and Cognitive Biology, University of Vienna, and Konrad Lorenz Institute of Ethology, University of Veterinary Medicine, Vienna.
¹³ Department of Biology, Millersville University, Millersville, PA 17551, USA.
¹⁴ Department of Biology, Loyola University Chicago, Chicago, IL 60660, USA.
¹⁵ Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR 97239, USA.
¹⁶ Cornell Lab of Ornithology, Ithaca, NY 14853, USA.
¹⁷ Cornell Lab of Ornithology, Ithaca, NY 14853, USA; Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA.
¹⁸ Computational Biology Department, Carnegie Melon University, Pittsburgh, PA 15213, USA.
¹⁹ Department of Physiology and Integrative Biology, University of California, Los Angeles, CA 90095, USA.
²⁰ Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA; Department of Physiology and Integrative Biology, University of California, Los Angeles, CA 90095, USA; Smithsonian Tropical Research Institute, Panama City, Panama. Electronic address: schlinge@lifesci.ucla.edu.

PMID: 36933440
DOI: 10.1016/j.yhbeh.2023.105340

Abstract

Organismal behavior, with its tremendous complexity and diversity, is generated by numerous physiological systems acting in coordination. Understanding how these systems evolve to support differences in behavior within and among species is a longstanding goal in biology that has captured the imagination of researchers who work on a multitude of taxa, including humans. Of particular importance are the physiological determinants of behavioral evolution, which are sometimes overlooked because we lack a robust conceptual framework to study mechanisms underlying adaptation and diversification of behavior. Here, we discuss a framework for such an analysis that applies a "systems view" to our understanding of behavioral control. This approach involves linking separate models that consider behavior and physiology as their own networks into a singular vertically integrated behavioral control system. In doing so, hormones commonly stand out as the links, or edges, among nodes within this system. To ground our discussion, we focus on studies of manakins (Pipridae), a family of Neotropical birds. These species have numerous physiological and endocrine specializations that support their elaborate reproductive displays. As a result, manakins provide a useful example to help imagine and visualize the way systems concepts can inform our appreciation of behavioral evolution. In particular, manakins help clarify how connectedness among physiological systems-which is maintained through endocrine signaling-potentiate and/or constrain the evolution of complex behavior to yield behavioral differences across taxa. Ultimately, we hope this review will continue to stimulate thought, discussion, and the emergence of research focused on integrated phenotypes in behavioral ecology and endocrinology.

Keywords: Adaptive evolution; Androgenic hormones; Animal behavior; Manakin birds; Organismal physiology; Robustness; Systems biology.

Publication types

Review
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Adaptation, Physiological
Animals
Endocrine System
Hormones
Humans
Passeriformes* / physiology
Systems Biology*

Substances

Hormones