A framework for studying behavioral evolution by reconstructing ancestral repertoires
Abstract
Although different animal species often exhibit extensive variation in many behaviors, typically scientists examine one or a small number of behaviors in any single study. Here, we propose a new framework to simultaneously study the evolution of many behaviors. We measured the behavioral repertoire of individuals from six species of fruit flies using unsupervised techniques and identified all stereotyped movements exhibited by each species. We then fit a Generalized Linear Mixed Model to estimate the intra- and inter-species behavioral covariances, and, by using the known phylogenetic relationships among species, we estimated the (unobserved) behaviors exhibited by ancestral species. We found that much of intra-specific behavioral variation has a similar covariance structure to previously described long-time scale variation in an individual’s behavior, suggesting that much of the measured variation between individuals of a single species in our assay reflects differences in the status of neural networks, rather than genetic or developmental differences between individuals. We then propose a method to identify groups of behaviors that appear to have evolved in a correlated manner, illustrating how sets of behaviors, rather than individual behaviors, likely evolved. Our approach provides a new framework for identifying co-evolving behaviors and may provide new opportunities to study the mechanistic basis of behavioral evolution.
Data availability
All behavioral region information is submitted with the article and will be posted publically, if accepted, on GitHub (https://github.com/bermanlabemory/behavioral-evolution). The original video data are too large to post (tens of TB), but will be made available upon request.
Article and author information
Author details
Funding
National Institute of Mental Health (MH115831-01)
- Gordon J Berman
Human Frontiers Science Program (RGY0076/2018)
- Gordon J Berman
Howard Hughes Medical Institute
- Jessica Cande
- David Stern
- Gordon J Berman
Research Corporation for Science Advancement (25999)
- Gordon J Berman
National Science Foundation (1806833)
- Catalina Rivera
Ministerio de Ciencia y Tecnología, Gobierno de la Provincia de Córdoba
- Damián G Hernández
The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jesse H Goldberg, Cornell University, United States
Version history
- Preprint posted: July 17, 2020 (view preprint)
- Received: August 5, 2020
- Accepted: September 1, 2021
- Accepted Manuscript published: September 2, 2021 (version 1)
- Version of Record published: September 16, 2021 (version 2)
Copyright
© 2021, Hernández et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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The genomes of close unicellular relatives of animals encode orthologs of many genes that regulate animal development. However, little is known about the function of such genes in unicellular organisms or the evolutionary process by which these genes came to function in multicellular development. The Hippo pathway, which regulates cell proliferation and tissue size in animals, is present in some of the closest unicellular relatives of animals, including the amoeboid organism Capsaspora owczarzaki. We previously showed that the Capsaspora ortholog of the Hippo pathway nuclear effector Yorkie/YAP/TAZ (coYki) regulates actin dynamics and the three-dimensional morphology of Capsaspora cell aggregates, but is dispensable for cell proliferation control (Phillips et al., 2022). However, the function of upstream Hippo pathway components, and whether and how they regulate coYki in Capsaspora, remained unknown. Here, we analyze the function of the upstream Hippo pathway kinases coHpo and coWts in Capsaspora by generating mutant lines for each gene. Loss of either kinase results in increased nuclear localization of coYki, indicating an ancient, premetazoan origin of this Hippo pathway regulatory mechanism. Strikingly, we find that loss of either kinase causes a contractile cell behavior and increased density of cell packing within Capsaspora aggregates. We further show that this increased cell density is not due to differences in proliferation, but rather actomyosin-dependent changes in the multicellular architecture of aggregates. Given its well-established role in cell density-regulated proliferation in animals, the increased density of cell packing in coHpo and coWts mutants suggests a shared and possibly ancient and conserved function of the Hippo pathway in cell density control. Together, these results implicate cytoskeletal regulation but not proliferation as an ancestral function of the Hippo pathway kinase cascade and uncover a novel role for Hippo signaling in regulating cell density in a proliferation-independent manner.
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