A simple mechanism for complex social behavior

Katie Parkinson, Neil J Buttery, Jason B Wolf, Christopher R L Thompson

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.
Original languageEnglish
Article numbere1001039
Number of pages15
JournalPLoS Biology
Volume9
Issue number3
DOIs
Publication statusPublished - 29 Mar 2011

Fingerprint

Social Behavior
social behavior
Dictyostelium discoideum
Dictyostelium
Amoeba
Molecular modeling
Genetic Selection
molecular genetics
cooperatives
Cooperative Behavior
natural selection
Molecular Biology
mathematical models
Genes
Costs and Cost Analysis
mutants
genetic variation
Costs
genes
testing

Cite this

Parkinson, K., Buttery, N. J., Wolf, J. B., & Thompson, C. R. L. (2011). A simple mechanism for complex social behavior. PLoS Biology, 9(3), [e1001039]. https://doi.org/10.1371/journal.pbio.1001039

A simple mechanism for complex social behavior. / Parkinson, Katie; Buttery, Neil J; Wolf, Jason B; Thompson, Christopher R L.

In: PLoS Biology, Vol. 9, No. 3, e1001039, 29.03.2011.

Research output: Contribution to journalArticle

Parkinson, K, Buttery, NJ, Wolf, JB & Thompson, CRL 2011, 'A simple mechanism for complex social behavior', PLoS Biology, vol. 9, no. 3, e1001039. https://doi.org/10.1371/journal.pbio.1001039
Parkinson, Katie ; Buttery, Neil J ; Wolf, Jason B ; Thompson, Christopher R L. / A simple mechanism for complex social behavior. In: PLoS Biology. 2011 ; Vol. 9, No. 3.
@article{63c1399720104cda9c79226375c00400,
title = "A simple mechanism for complex social behavior",
abstract = "The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.",
author = "Katie Parkinson and Buttery, {Neil J} and Wolf, {Jason B} and Thompson, {Christopher R L}",
year = "2011",
month = "3",
day = "29",
doi = "10.1371/journal.pbio.1001039",
language = "English",
volume = "9",
journal = "PLOS Biology",
issn = "1545-7885",
publisher = "Public Library of Science (PLOS)",
number = "3",

}

TY - JOUR

T1 - A simple mechanism for complex social behavior

AU - Parkinson, Katie

AU - Buttery, Neil J

AU - Wolf, Jason B

AU - Thompson, Christopher R L

PY - 2011/3/29

Y1 - 2011/3/29

N2 - The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.

AB - The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.

UR - http://www.scopus.com/inward/record.url?scp=79953686813&partnerID=8YFLogxK

UR - http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3066132/

UR - http://dx.doi.org/10.1371/journal.pbio.1001039

U2 - 10.1371/journal.pbio.1001039

DO - 10.1371/journal.pbio.1001039

M3 - Article

VL - 9

JO - PLOS Biology

JF - PLOS Biology

SN - 1545-7885

IS - 3

M1 - e1001039

ER -