Massive horizontal gene transfer and the evolution of nematomorph-driven behavioral manipulation of mantids

To complete their life cycle, a wide range of parasites must manipulate the behavior of their hosts. 1 Hughes D.P. Libersat F. Parasite manipulation of host behavior. Curr. Biol. 2019; 29: R45-R47 Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar This manipulation is a well-known example of the “extended phenotype, 2 Dawkins R. The extended phenotype: The long reach of the gene. Oxford University Press, 1999 Google Scholar ” where genes in one organism have phenotypic effects on another organism. Recent studies have explored the parasite genes responsible for such manipulation of host behavior, including the potential molecular mechanisms. 3 Hoover K. Grove M. Gardner M. Hughes D.P. McNeil J. Slavicek J. A gene for an extended phenotype. Science. 2011; 333: 1401 Crossref PubMed Scopus (165) Google Scholar ,4 Katsuma S. Koyano Y. Kang W. Kokusho R. Kamita S.G. Shimada T. The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Path. 2012; 8e1002644 Crossref PubMed Scopus (67) Google Scholar However, little is known about how parasites have acquired the genes involved in manipulating phylogenetically distinct hosts. 4 Katsuma S. Koyano Y. Kang W. Kokusho R. Kamita S.G. Shimada T. The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Path. 2012; 8e1002644 Crossref PubMed Scopus (67) Google Scholar In a fascinating example of the extended phenotype, nematomorph parasites have evolved the ability to induce their terrestrial insect hosts to enter bodies of water, where the parasite then reproduces. Here, we comprehensively analyzed nematomorphs and their mantid hosts, focusing on the transcriptomic changes associated with host manipulations and sequence similarity between host and parasite genes to test molecular mimicry. The nematomorph’s transcriptome changed during host manipulation, whereas no distinct changes were found in mantids. We then discovered numerous possible host-derived genes in nematomorphs, and these genes were frequently up-regulated during host manipulation. Our findings suggest a possible general role of horizontal gene transfer (HGT) in the molecular mechanisms of host manipulation, as well as in the genome evolution of manipulative parasites. The evidence of HGT between multicellular eukaryotes remains scarce but is increasing and, therefore, elucidating its mechanisms will advance our understanding of the enduring influence of HGT on the evolution of the web of life.