Into the wild: a long-term study of begomovirus community dynamics in a natural landscape

Begomoviruses have been the subject of many evolutionary studies that explored their temporal dynamics; however, most of the studies relied on sequences retrieved from public repositories rather than hypothesis-driven sampling. These datasets are often temporally or spatially unbalanced, which can bias molecular clock calibration, especially when the population exhibits strong genetic structure. Furthermore, most studies have focused on agricultural environments where anthropogenic activity may influence viral diversification. Longitudinal studies with systematic sampling in the natural environment are essential to understand begomovirus ecology and evolution. We monitored a begomovirus community over 12 years (2011-2014, 2016-2022) in a 300 m² Atlantic Forest regeneration area in southeastern Brazil, sampling 385 Sida acuta plants and obtaining 371 complete genomic segments (262 DNA-A and 109 DNA-B). We quantified community diversity and estimated substitution rates and demographic dynamics. Five begomoviruses were detected at the site, with Oxalis yellow vein virus (OxYVV; Begomovirus oxalisflavi) and Sida yellow leaf curl virus (SiYLCV; Begomovirus sidaflavacontorsionis) dominating the community. Species composition changed over time: OxYVV was the most frequent virus during the early years but was outnumbered by SiYLCV from 2016 onwards, with alternating prevalence in later years. Community diversity peaked in 2021 when all five viruses were detected co-occurring. The diversification of SiYLCV exhibited a higher relative contribution of recombination than mutation (ρ/θ>1), contrary to all other begomoviruses studied to date. Although we hypothesized that the changes in community composition observed in 2016 resulted from a genetic bottleneck in the OxYVV population, no evidence of such an event was detected. Instead, we observed a demographic expansion of SiYLCV, consistent with its increase in frequency. This study reveals the complex community dynamics of begomoviruses in natural landscapes and underscores the role of wild plants as reservoirs of viral diversity, providing a baseline for comparisons with agroecosystems to inform management strategies.