Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes

Abstract

AbstractThe transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. After the establishment of antagonistic relationships, parasites and hosts co-evolve through reciprocal adaptations, often resulting in evolutionary arms-races. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine those gene expression patterns that characterize slavemaker raiding and reciprocal host defensive phenotypes. Previous behavioural studies have established that raiding strategies between Temnothorax slavemakers diverge, while host defense portfolios shift similarly under parasite pressure. We are the first to confirm this at the molecular level, revealing that slavemaking species exhibit a wider variety of genes with species-specific patterns of expression within their raiding phenotypes, whereas expression similarity is commonly found during the non-raiding phenotype. Host species response to slavemaker aggression, however, is indicated by strong changes in the expression of a relatively few number genes. Additionally, the expression of individual genes such as Acyl-CoA-Delta(11) desaturase and Trypsin-7 is strongly associated with the raiding phenotype of all three slavemaking species. Here, we provide novel insight into the gene expression patterns associated with raiding and nest defense behavior in Temnothorax ants, suggesting lineage-specific evolutionary patterns among both slavemakers and hosts.

Autoren

Austin Alleman
Barbara Feldmeyer
Susanne Foitzik

DOI

10.1038/s41598-018-20262-y

eISSN

2045-2322

Ausgabe der Veröffentlichung

1

Zeitschrift

Scientific Reports

Sprache

en

Artikelnummer

1951

Online publication date

2018

Status

Published online

Herausgeber

Springer Science and Business Media LLC

Herausgeber URL

http://dx.doi.org/10.1038/s41598-018-20262-y

Datum der Datenerfassung

2022

Titel

Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes

Ausgabe der Zeitschrift

8

Data source: Crossref

Abstract

The transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. After the establishment of antagonistic relationships, parasites and hosts co-evolve through reciprocal adaptations, often resulting in evolutionary arms-races. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine those gene expression patterns that characterize slavemaker raiding and reciprocal host defensive phenotypes. Previous behavioural studies have established that raiding strategies between Temnothorax slavemakers diverge, while host defense portfolios shift similarly under parasite pressure. We are the first to confirm this at the molecular level, revealing that slavemaking species exhibit a wider variety of genes with species-specific patterns of expression within their raiding phenotypes, whereas expression similarity is commonly found during the non-raiding phenotype. Host species response to slavemaker aggression, however, is indicated by strong changes in the expression of a relatively few number genes. Additionally, the expression of individual genes such as Acyl-CoA-Delta(11) desaturase and Trypsin-7 is strongly associated with the raiding phenotype of all three slavemaking species. Here, we provide novel insight into the gene expression patterns associated with raiding and nest defense behavior in Temnothorax ants, suggesting lineage-specific evolutionary patterns among both slavemakers and hosts.

Addresses

Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Johannes von Müller Weg 6, Mainz, 55128, Germany. aalleman@uni-mainz.de.

Autoren

Austin Alleman
Barbara Feldmeyer
Susanne Foitzik

DOI

10.1038/s41598-018-20262-y

eISSN

2045-2322

Externe Identifier

PubMed Identifier: 29386535
PubMed Central ID: PMC5792630

Open access

true

ISSN

2045-2322

Ausgabe der Veröffentlichung

1

Zeitschrift

Scientific reports

Schlüsselwörter

Animals
Ants
Likelihood Functions
Sequence Analysis, RNA
Phylogeny
Species Specificity
Gene Expression Regulation
Up-Regulation
Phenotype
Gene Regulatory Networks
Host-Parasite Interactions
Biological Evolution
Transcriptome

Sprache

eng

Medium

Electronic

Online publication date

2018

Open access status

Open Access

Paginierung

1951

Datum der Veröffentlichung

2018

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2018

Titel

Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes.

Sub types

Comparative Study
Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

8

Files

https://www.nature.com/articles/s41598-018-20262-y.pdf https://europepmc.org/articles/PMC5792630?pdf=render

Data source: Europe PubMed Central

Abstract

The transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. After the establishment of antagonistic relationships, parasites and hosts co-evolve through reciprocal adaptations, often resulting in evolutionary arms-races. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine those gene expression patterns that characterize slavemaker raiding and reciprocal host defensive phenotypes. Previous behavioural studies have established that raiding strategies between Temnothorax slavemakers diverge, while host defense portfolios shift similarly under parasite pressure. We are the first to confirm this at the molecular level, revealing that slavemaking species exhibit a wider variety of genes with species-specific patterns of expression within their raiding phenotypes, whereas expression similarity is commonly found during the non-raiding phenotype. Host species response to slavemaker aggression, however, is indicated by strong changes in the expression of a relatively few number genes. Additionally, the expression of individual genes such as Acyl-CoA-Delta(11) desaturase and Trypsin-7 is strongly associated with the raiding phenotype of all three slavemaking species. Here, we provide novel insight into the gene expression patterns associated with raiding and nest defense behavior in Temnothorax ants, suggesting lineage-specific evolutionary patterns among both slavemakers and hosts.

Date of acceptance

2018

Autoren

Austin Alleman
Barbara Feldmeyer
Susanne Foitzik

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/29386535

DOI

10.1038/s41598-018-20262-y

eISSN

2045-2322

Externe Identifier

PubMed Central ID: PMC5792630

Ausgabe der Veröffentlichung

1

Zeitschrift

Sci Rep

Schlüsselwörter

Animals
Ants
Biological Evolution
Gene Expression Regulation
Gene Regulatory Networks
Host-Parasite Interactions
Likelihood Functions
Phenotype
Phylogeny
Sequence Analysis, RNA
Species Specificity
Transcriptome
Up-Regulation

Sprache

eng

Country

England

Paginierung

1951

PII

10.1038/s41598-018-20262-y

Datum der Veröffentlichung

2018

Status

Published online

Datum, an dem der Datensatz öffentlich gemacht wurde

2018

Titel

Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes.

Sub types

Comparative Study
Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

8

Data source: PubMed

Author's licence

CC-BY

Autoren

Austin Alleman
Barbara Feldmeyer
Susanne Foitzik

Hosting institution

Universitätsbibliothek Mainz

Sammlungen

JGU-Publikationen

Resource version

Published version

DOI

10.1038/s41598-018-20262-y

Funding acknowledgements

DFG, Open Access-Publizieren Universität Mainz / Universitätsmedizin

File(s) embargoed

false

Open access

true

ISSN

2045-2322

Zeitschrift

Scientific reports

Schlüsselwörter

570 Biowissenschaften
570 Life sciences

Sprache

eng

Open access status

Open Access

Paginierung

Art. 1951

Datum der Veröffentlichung

2018

Public URL

https://openscience.ub.uni-mainz.de/handle/20.500.12030/573

Herausgeber

Macmillan Publishers Limited, part of Springer Nature

Herausgeber URL

http://dx.doi.org/10.1038/s41598-018-20262-y

Datum der Datenerfassung

2018

Datum, an dem der Datensatz öffentlich gemacht wurde

2018

Zugang

Public

Titel

Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes

Ausgabe der Zeitschrift

8

Files

58086.pdf

Data source: OPENSCIENCE.UB

Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes

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