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

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.

SUBMITTER: Alleman A

PROVIDER: S-EPMC5792630 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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

Alleman Austin A Feldmeyer Barbara B Foitzik Susanne S

Scientific reports 20180131 1

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. Pr ...[more]

PMID: 29386535

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Project description:Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the "Enemy Hypothesis," which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.

Dataset Information

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

Publications

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

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