Genomic Insights into Vector-Pathogen Adaptation in Haemaphysalis longicornis and Rhipicephalus microplus

Abstract

As crucial vectors that transmit pathogens to humans and livestock, ticks pose substantial global health threats and economic burdens. We analyzed 328 tick genomes to explore the population's genetic structure and the adaptive evolution of H. longicornis and R. microplus, two tick species with distinct life cycle characteristics. We observed distinct genetic structures in H. longicornis and R. microplus. Gene flow estimation revealed a closer genetic connection in R. microplus than H. longicornis, which was facilitated by geographical proximity. Notably, we identified a set of candidate genes associated with possible adaptations. Specifically, the immune-related gene DUOX and the iron transport gene ACO1 showed significant signals of natural selection in R. microplus. Similarly, H. longicornis exhibited selection in pyridoxal-phosphate-dependent enzyme genes associated with heme synthesis. Moreover, we observed significant correlations between the abundance of pathogens, such as Rickettsia and Francisella, and specific tick genotypes, which highlights the role of R. microplus in maintaining these pathogens and its adaptations that influence immune responses and iron metabolism, suggesting potential coevolution between vectors and pathogens. Our study highlights the vital genes involved in tick blood feeding and immunity, and it provides insights into the coevolution of ticks and tick-borne pathogens.

Keywords: Haemaphysalis longicornis; Rhipicephalus microplus; tick-borne disease; vector–pathogen adaptation.

Figure 1

Population structures of H. longicornis and R. microplus. (A,B) Principal component analysis (PCA) plot showing segregation of H. longicornis and R. microplus individuals, respectively. Differently colored shapes represent samples from different populations and provinces. SCC, South Central China; SEC, Southeast China; SWC, Southwest China. (C) Phylogenetic structure of R. microplus populations. (D) Population genetic structure of all R. microplus sample accessions, as estimated using ADMIXTURE with the best K = 2. The outer circle graphic shows the ancestry proportions of each individual, and the center pie chart highlights the ancestry proportions of the SEC population. Each color represents a different ancestral composition. (E,F) LD decay in different populations of H. longicornis and R. microplus.

Figure 2

Gene diversity and gene flow of H. longicornis and R. microplus in different geographical regions. (A) Regional distribution of the two tick species in China. (B) Tajima’s D values of the two tick species in different regions. (C) Gene flow between the different regions for R. microplus populations. (D) Migratory patterns of R. microplus based on EEMS (estimated effective migration surface).

Figure 3

DUOX gene and ACO1 gene contribution to blood digestion and the immune response of R. microplus. (A) Whole-genome scan with F_ST and iHS for the SNPs around DUOX, ACO1, and Vacuolar H+ ATPases between the Southeast China (SEC) and Southwest China (SWC) populations. F_ST is normalized as Z scores for R. microplus. The horizontal red dashed lines represent the empirical threshold for the selected regions. (B) Genotype frequency of rs142127589 among the three R. microplus populations. (C) Correlation of a DUOX SNP (rs142127589) with the abundance of Rickettsias. (D) Haplotype decay around the DUOX-chr9-142127589 allele in SEC and SWC populations. (E) Gene expression of the DUOX gene in different tissues or development stages. Digestive cells from fully engorged female ticks (DIG_F); fat bodies from partially and fully engorged adult females (FB); synganglion from partially and fully engorged adult females (SYN); digestive cells from partially engorged female ticks (DIG_P); embryos (EMB); ovaries from partially and fully engorged adult females (OV); salivary glands from partially and fully engorged adult females (SG). (F) Alternative allele frequency across the three R. microplus populations. (G) Gene expression of ACO1 gene in different tissues or development stages. (H) Life circle of R. microplus blood meal digestion. (I) The DUOX gene contributes to blood digestion and the immune response in R. microplus.

Figure 4

PLP-dependent enzyme gene contributes to blood digestion in H. longicornis. (A) Whole-genome scan with iHS: top 1% windows; the horizontal red dashed lines represent the empirical threshold for the selected regions. (B) Genotype frequency of rs65770851 across H. longicornis populations. (C) Correlation of a PLP-dependent enzyme SNP (rs65770851) with the abundance of Coxiella. (D) PLP-dependent enzymes in nymphs treated with tetracycline (TET) versus controls (CT) (E) PLP-dependent enzyme genes contributing to blood digestion and heme synthesis in H. longicornis.

Figure 5

The tick genetic variant rs88416395 is correlated with the abundance of tick-borne pathogens. (A–C) Correlation of a Toll-like receptors SNP (rs88418395) with Rickettsia, Bartonella, and Francisella abundance, respectively. (D) Genotype frequency of rs88418395 among the SCC, SEC, and SWC populations.