Eco-evolutionary dynamics of a shifting porcine parvoviruses (PPV1–PPV8) ecosystem reveal dichotomous selection pressures

Porcine parvoviruses (PPVs) constitute a complex viral ecosystem. However, the genetic structure and evolutionary dynamics of currently circulating PPV populations remain poorly characterized. A large-scale genomic survey in China (1,055 genomes; 863 samples; 2021-2024) reveal a profound ecosystem shift, with PPVs detected in 212/863 samples (24.57%) Novel species (PPV7, 16.45%; PPV6, 9.62%; and PPV2, 8.82%) now dominate the niche previously occupied by classical PPV1 (3.13%). This new landscape is defined by pervasive multi-species co-infection (129/212, 60.85%), including 61 cases with ≥ 3 species and 7 pigs co-infected with ≥ 5 species, characterized by non-random associations, where even low-prevalence species such as PPV1 and PPV5 exhibit a high propensity for co-infection (permutation test: PPV1 p < 0.001; PPV5 p = 0.002). This high-transmission environment provides ample opportunities for frequent intra-species recombination, which powerfully accelerates variation within the primary antigenic region (ORF2). This study uncovered dichotomous evolutionary dynamics driven by contrasting immune pressure. The dominant naturally circulating species were constrained by strong purifying selection. In stark contrast, vaccine-targeted PPV1 followed a distinct path driven by strong positive selection of key surface epitopes (e.g., VP2 site 435), suggesting an adaptation to evade vaccine-induced immunity. Collectively, our work deconstructs how natural selection and vaccine filtering impose distinct selective regimes on the viral population, establishing a new framework for evolutionarily aware surveillance and rational design of next-generation vaccines.