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.
Highlights
Understanding the processes that shape the evolutionary trajectories of organisms is a long-standing goal of the biological sciences
Finalized transcriptomes vary from 43,664 contigs (T. ambiguus) to 79,227 contigs (T. curvispinosus), with N50 values ranging from 2,973 to 3,606 (Supplementary Table S2)
A total of 3,381 genes were found to be differently-expressed between these two phenotypes of the slavemakers (T. americanus: 975, T. duloticus: 890, and T. pilagens: 1616; Fig. 2) and 697 genes differentially-expressed within the hosts’ two phenotypes (T. longispinosus: 209, T. curvispinosus: 108, and T. ambiguus: 380; Fig. 2; complete lists contained in Supplementary Tables S3 and S4)
Summary
Understanding the processes that shape the evolutionary trajectories of organisms is a long-standing goal of the biological sciences. In addition to slavemaker-specific morphological characteristics such as powerful mandibles[22,23], potent stingers[23,24], and enlarged petioles[25], slavemakers often employ the Dufour’s gland and other glandular secretions to manipulate hosts[30,31], mimic host profiles[32], or obtain recognition cues directly from hosts in order to camouflage themselves[33] This rapid diversification of species-specific mechanisms and strategies within social parasites is a direct indication of (3) increased phenotypic diversity, a result of loosened phenotypic constraints associated with the transition away from a free-living lifestyle[34]. In those raids where it is recognized as an enemy, T. pilagens responds violently to host attacks, stinging defending hosts and imparting high mortality upon the host colony[24]
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