Signatures of co-evolutionary host-pathogen interactions in the genome of the entomopathogenic nematode Steinernema carpocapsae

Abstract

BackgroundThe entomopathogenic nematode Steinernema carpocapsae has been used worldwide as a biocontrol agent for insect pests, making it an interesting model for understanding parasite-host interactions. Two models propose that these interactions are co-evolutionary processes in such a way that equilibrium is never reached. In one model, known as “arms race”, new alleles in relevant genes are fixed in both host and pathogens by directional positive selection, producing recurrent and alternating selective sweeps. In the other model, known as“trench warfare”, persistent dynamic fluctuations in allele frequencies are sustained by balancing selection. There are some examples of genes evolving according to both models, however, it is not clear to what extent these interactions might alter genome-level evolutionary patterns and intraspecific diversity. Here we investigate some of these aspects by studying genomic variation in S. carpocapsae and other pathogenic and free-living nematodes from phylogenetic clades IV and V.ResultsTo look for signatures of an arms-race dynamic, we conducted massive scans to detect directional positive selection in interspecific data. In free-living nematodes, we detected a significantly higher proportion of genes with sites under positive selection than in parasitic nematodes. However, in these genes, we found more enriched Gene Ontology terms in parasites. To detect possible effects of dynamic polymorphisms interactions we looked for signatures of balancing selection in intraspecific genomic data. The observed distribution of Tajima’s D values in S. carpocapsae was more skewed to positive values and significantly different from the observed distribution in the free-living Caenorhabditis briggsae. Also, the proportion of significant positive values of Tajima’s D was elevated in genes that were differentially expressed after induction with insect tissues as compared to both non-differentially expressed genes and the global scan.ConclusionsOur study provides a first portrait of the effects that lifestyle might have in shaping the patterns of selection at the genomic level. An arms-race between hosts and pathogens seems to be affecting specific genetic functions but not necessarily increasing the number of positively selected genes. Trench warfare dynamics seem to be acting more generally in the genome, likely focusing on genes responding to the interaction, rather than targeting specific genetic functions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0935-x) contains supplementary material, which is available to authorized users.

Insect immunity - adaptive mechanisms and survival strategies

“…Zmiany te mogą mieć charakter szybko wprowadzanych zarówno na poziomie genetycznym jaki i epigenetycznym. Nowe allele "genów adaptacji" przekazywane są zarówno w populacji drapieżnika i ofiary, prowadzą kierunkową selekcję pozytywną, a cykliczność procesu prowadzi do nieustannej presji na każdego z przeciwników [106,109]. Ze względu na dużą skalę nakładów energetycznych do prowadzenia ciągłego "dozbrajania" każdego z przeciwników "wyścig zbrojeń" nie może być procesem trwającym w nieskończoność.…”

“…W odpowiedzi, w populacji ofiary pojawia się "gen odporności", którego częstotliwość w populacji wzrasta, w skutek czego posiadanie przez drapieżnika "genu wirulencji" nie przynosi mu korzyści i częstotliwość jego występowania w populacji spada. Wraz ze wzrostem liczby osobników danej populacji posiadających allel niosący cechę kontradaptacyjną, przewaga zmniejsza się [109,111]. Analizując strategię owada w odpowiedzi na zakażenie patogenem, szczególną uwagę należy zwrócić na wydatki energetyczne jakie musi ponieść gospodarz, aby przeprowadzić skuteczną obronę organizmu.…”

ShK-Domain-Containing Protein from a Parasitic Nematode Modulates Drosophila melanogaster Immunity

“…Entomopathogenic nematodes (EPNs) are used in integrated pest management [ 9 , 10 , 11 ]. EPNs are also regarded as a model system and are widely used in evolutionary biology, biological control, symbiosis, soil ecology, and neurobiology [ 12 , 13 , 14 , 15 , 16 ].…”