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Comparative analysis of co-evolving host-parasite associations reveal unique expression patterns and pathways underlying slavemaker raiding and host defensive behavior in ants

ABSTRACT: The transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. Evolutionarily 'young' parasites are ideal models for the elucidation of the early steps of this transition. After the establishment of an antagonistic relationship, parasite and host co-evolve through reciprocal adaptations resulting in an evolutionary arms-race. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine gene expression patterns characterizing slavemaker raiding and reciprocal host defensive behavior. Previous studies of Temnothorax provide evidence for co-evolving adaptations between parasites and hosts, as well as diverging raiding strategies between slavemakers. However, under parasite pressure, host defense portfolios shift similarly, suggesting diverging evolution of defensive traits. Through comparative gene expression analyses, we find that slavemaker raiding behavior is characterized by a down-regulation of numerous genes relative to their non-raiding state. Moreover, only a small number of genes shared expression between slavemaking species. In contrast, hosts possess a higher ratio of commonly-to-privately over-expressed genes and metabolic pathways during raids, suggesting that genes of similar function control defensive behavior. Additionally, a number of candidate genes were identified, each potentially playing a major role in shaping slavemaker- and host-specific behaviors. Finally, in two slavemaking species, functional enrichment analyses indicate that genes over-expressed during raiding behavior are associated with ribosomal structure, oxidation-reduction, and metabolic processes. Overall, our analysis revealed evidence for divergent evolution among closely-related ant species, where species-specific gene expression characterize raiding and defensive behavior.

ORGANISM(S): Temnothorax curvispinosus Temnothorax pilagens Temnothorax americanus Temnothorax duloticus Temnothorax ambiguus Temnothorax longispinosus

PROVIDER: GSE95604 | GEO | 2017/07/01

SECONDARY ACCESSION(S): PRJNA377627

REPOSITORIES: GEO

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Project description:We found that assassin bugs from the earliest-diverging subfamily of higher Reduviidae (Peiratinae), as well as a subfamily closely related to Triatominae (Stenopodainae) have venom that is highly similar in composition to that produced by previously examined reduviids from Harpactorinae and Reduviinae. This finding suggests that venom composition has been largely stable due to purifying selection among the higher Reduviidae, which is consistent with the ancient origin of venom in the ancestors of Heteroptera 250–300 million years ago (Sunagar and Moran 2015; Walker et al. 2018a). This near homogeneity of venom composition is perhaps surprising considering that reduviid predators have evolved numerous instances of prey specialization and specialized hunting strategies that might be expected to co-evolve with venom. Possibly, further studies focussing on species with more specialized hunting strategies, or different kinds of venom bioactivities, will uncover more nuanced venom adaptations. Alternatively, it is possible that the protease-rich venoms of predatory reduviids are simply well-suited to myriad different hunting strategies. These data are consistent with other examples where venoms are surprisingly similar despite great differences in biology, for example between solitary and eusocial bees. A more detailed picture of venom evolution in Reduviidae would examine venom produced by the early-diverging Phymatine complex as well as venoms of non-reduviid cimicomorphs, prey specialists such as the arachnophagous Emesinae and the myrmecophagous Holoptilinae, and some of the many groups that employ hunting specializations, such as the use of plant resins to catch prey (Hwang and Weirauch 2012). Within Triatominae, examination of saliva produced by additional species from multiple lineages (especially those that switched to blood-feeding independently, if the subfamily is shown to be polyphyletic) and including generalists and specialists on different host taxa and species associated especially with nests and burrows will be informative. The venoms of predatory reduviids such as Zelurus spp. and Opisthacidius spp. that are most closely related to Triatominae, and share some behaviours such as habitation of bird nests by Opisthacidius spp. may also provide more information about the evolution of triatomine saliva.

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Comparative analysis of co-evolving host-parasite associations reveal unique expression patterns and pathways underlying slavemaker raiding and host defensive behavior in ants

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