Comparative mitogenomics reveals evolutionary drivers of Strongyloidea nematodes dwelling in gastrointestinal tract

Abstract

Background: The nematode superfamily Strongyloidea represents a prevalent group of gastrointestinal parasites in ruminants and livestock, posing substantial veterinary and economic burdens worldwide. Here we present the first mitochondrial genomic investigation for reconstructing Strongyloidea phylogeny and investigating niche-specific selection dynamics across gastrointestinal habitats (abomasum, small intestine, and large intestine). This study presents a preliminary exploration of the evolutionary adaptations of these agriculturally relevant parasites through comprehensive mitogenomic analysis.

Results: Phylogenomic reconstruction revealed strong anatomical clustering with high nodal support. Comparative synteny analyses revealed conserved mitogenome architectures across Strongyloidea species, characterized by pronounced AT-richness. Codon usage patterns showed high consistency in Strongyloide (94% A/U-ending preferred codons), with ENC-plot and neutrality analyses confirming natural selection as the dominant driver. Pervasive purifying selection was observed, but abomasal species showed higher ω values than intestinal counterparts, particularly in ND4. In addition, positive selection was detected exclusively in CYTB within the small intestinal lineage. RELAX analysis identified differential selection signals among the three branches, with significant relaxation observed in ND5 and ND6 genes in the abomasal species. Amino acid polymorphism analyses revealed higher sequence variation in ND genes compared to the highly conserved COX genes.

Conclusions: Our findings demonstrated niche-associated evolutionary trajectories between abomasal and intestinal Strongyloidea branches, reflected in both phylogenetic patterns and molecular evolution rates. The mitogenomic framework established here provided a foundation for future studies integrating expanded datasets, genomic data, and microenvironmental parameters to elucidate precise niche adaptation mechanisms in these economically important parasites.

Keywords: Abomasum; Large intestine; Mitochondrial genome; Phylogenetic relationships; Selection pressure; Small intestine; Strongyloidea.

Fig. 1

Heterogeneity analysis based on different datasets. The mean similarity score between sequences was depicted by a colored square using AliGROOVE analysis. Score values ranged from − 1, indicating great difference in rates from the remainder of the datasets (high heterogeneity, red coloration), to + 1, indicating similarity to all other comparisons (low heterogeneity, blue coloration)

Fig. 2

Phylogenetic relationships and mitogenomic collinearity analysis. A Phylogenetic relationships inferred from ML and BI analysis based on the AA, PCG123, PCG12, and PCG1 datasets. The values at the nodes represent BI posterior probabilities, SH-aLRT, UFBoot supports, and sCF, respectively. For PCG1 matrix, the presented topology was supported exclusively under the Bayesian inference model. Phylogenetic branches were color-coded according to parasite localization: red for abomasum-parasitizing species, blue for small intestine-parasitizing species, and green for large intestine-parasitizing species. B Synteny blocks were represented by gray lines. The peaks illustrated the distribution of GC content throughout the mitogenome, with lines above the baseline representing regions exceeding 50% GC content, and lines below indicating regions with less than 50% GC content

Fig. 3

RSCU values and optimal codons analyses. A RSCU values of the codons in the mitogenomes of 12 Strongyloidea species. Blue to red indicated RSCU values from low to high. B Optimal codons in the mitogenomes of 12 Strongyloidea species. The bottom of the heatmap displayed the optimal codon and its corresponding encoded amino acid. The right bar plot represented the number of optimal codons in different species. The red boxes indicated the optimal codons present within the species

Fig. 4

ENC-GC3 plots of Strongyloidea species. The standard curve (blue line) indicated the expected codon usage if GC compositional constraints alone account for codon usage bias. Black dots represented the PCGs, with deviations from the curve suggesting additional pressures influencing codon usage bias

Fig. 5

Selective pressure and AA polymorphism analysis. A Comparisons of dN/dS ratios among three gastrointestinal niches based on all PCGs. B The dN/dS ratios of individual PCGs and concatenated 12 PCGs across three branches based on the free-ratio model. C Comparisons of frequencies of amino acid polymorphisms among three gastrointestinal niches based on all PCGs. D Frequencies of AA polymorphisms in individual PCGs and concatenated 12 PCGs across three branches. *: p value < 0.05; **: p value < 0.01; NS: not significant