Endemic persistence and invasive emergence: begomoviruses in Mexico

Begomoviruses, the whitefly-transmitted single-stranded DNA viruses of the genus Begomovirus in the family Geminiviridae, rank among the most economically damaging viral pathogens of tropical and subtropical agriculture. Yet, according to a new perspective article published in Frontiers in Virology, these globally important plant viruses have too often been studied through isolated, pathogen-centered case studies that miss the bigger picture. A team of Mexican researchers led by Katia Aviña-Padilla of the Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional and Alfredo Diaz-Lara of Tecnológico de Monterrey now proposes a conceptual eco-evolutionary framework in which begomoviruses in agroecosystems operate under two contrasting but interconnected regimes: endemic persistence and invasive emergence. The framework, grounded in decades of field and molecular evidence from Mexican pepper- and tomato-associated systems, aims to shift begomovirus management from reactive outbreak response toward anticipatory, risk-informed surveillance.

The distinction between the two regimes is central to the proposal. Endemic persistence describes viral systems that remain regionally established over long temporal scales, coexisting with local crops, weeds, and vector populations under relatively stable ecological interactions. Such systems are characterized by ecological continuity, recurrent mixed infections, local recombination, and long-term circulation within regional host–vector networks. Invasive emergence, by contrast, involves the biological introduction and rapid spatial expansion of viral lineages into novel agroecological contexts, frequently associated with shifts in vector populations, crop intensification, trade-mediated dispersal, and ecological disturbance, followed by strong anthropogenic selection and post-introduction adaptation. Importantly, the authors stress that these regimes are not mutually exclusive categories; rather, they coexist and interact within shared agricultural landscapes, creating opportunities for mixed infections, recombination, host shifts, and the generation of novel epidemiological trajectories.

To make the framework empirically useful, the researchers operationalize the endemic–invasive continuum along four measurable axes: temporal persistence, measured as years of documented regional circulation; geographic range breadth, measured as the number of distinct production regions with confirmed detection; mixed-infection frequency, measured as the proportion of field-collected samples co-infected by two or more begomovirus species; and recombination incidence, estimated from the frequency of recombination events detected per genomic dataset in published surveys. Under this scheme, the pepper huasteco yellow vein virus (PHYVV, Begomovirus capsicumhuastecoense) and pepper golden mosaic virus (PepGMV, B. capsicummusivi) rank high on the first three axes, consistent with long-term endemic persistence, whereas tomato yellow leaf curl virus (TYLCV, B. coheni) ranks high on geographic breadth, reflecting its rapid expansion, but lower on temporal persistence and mixed-infection frequency within Mexican systems, consistent with its recent introduction. The authors note that position along these axes is dynamic and may shift as ecological and epidemiological conditions change, reinforcing the continuum rather than categorical nature of the regimes. A formally weighted composite index is beyond the scope of the current perspective, but future work could normalize each axis to a 0–1 scale and combine them into a quantitative continuum-position score for tracking directional shifts over time.

Mexico provides an especially relevant empirical arena for the framework because its pepper- and tomato-associated agroecosystems contain both regionally persistent begomoviruses and recently introduced invasive lineages, all within highly connected production systems dominated by whitefly-mediated transmission. The authors use the PHYVV/PepGMV and TYLCV pathosystems as contrasting models of the two regimes. They also introduce the concept of surveillance-relevant contact zones: agroecological areas where endemic and invasive begomovirus regimes spatially or temporally co-occur within shared host and vector networks, thereby elevating the probability of mixed infection, genomic exchange, and the emergence of novel viral variants. Such zones may function as evolutionary interfaces that facilitate the appearance of variants with altered host range, transmission efficiency, or pathogenicity, making them priority locations for genomic monitoring.

The biological attributes of begomoviruses underpin the entire framework. These compact single-stranded DNA viruses mainly infect dicotyledonous plants and display either monopartite or bipartite genome organization, encoding functions required for replication, movement, encapsidation, and vector-mediated transmission while enabling rapid diversification through mutation, recombination, and genomic component exchange. Recombination is a major evolutionary process shaping begomovirus diversification: comparative analyses of DNA-A and DNA-A-like components have identified recombination hot- and cold-spots, suggesting that genomic exchange is constrained by functional and structural organization rather than occurring randomly. Phylogeographic analyses of coat protein and replication-associated protein sequences further reveal strong geographic structure among begomovirus populations, indicating that regional ecological conditions and dispersal histories contribute to diversification patterns. The whitefly vector itself is now recognized as a complex of cryptic lineages differing in geographic distribution, host range, transmission efficiency, and invasion potential, and through its vector activity it interconnects cultivated crops, weeds, ruderal vegetation, and alternative hosts within broader epidemiological networks.

Mixed infection adds another critical layer. Experimental studies have demonstrated synergistic interactions between PHYVV and PepGMV in pepper (Capsicum annuum) plants, resulting in increased symptom severity and viral DNA accumulation. Superinfection by PHYVV can additionally modify recovery responses in PepGMV-infected plants through changes in viral DNA accumulation, DNA methylation, and viral chromatin state. More recent studies indicate that coinfection and recombination may generate recombinant variants with altered competitive capacity and epidemiological behavior, reinforcing the importance of ecological contact zones where endemic and invasive viral lineages overlap. In Mexican pepper agroecosystems, field surveys in the state of Sinaloa revealed high prevalence of both endemic viruses in symptomatic chili pepper plants, with PHYVV detected in 74.4 percent and PepGMV in 53.7 percent of analyzed samples, including frequent PHYVV/PepGMV mixed infections. Experimental transmission assays have further shown that the whitefly can efficiently acquire and transmit both viruses individually or simultaneously to chili pepper plants, creating ecological conditions that facilitate coinfection and increase opportunities for viral interaction within shared hosts.

Evidence from Mexican chiltepin pepper-associated systems extends these findings to the eco-evolutionary scale. Rodelo-Urrego and colleagues showed that ecosystem biodiversity modulates PHYVV and PepGMV genetic diversity in a virus-specific manner while also detecting recombinant and reassortant viral variants. From this perspective, the authors cautiously interpret the PHYVV/PepGMV pathosystem as an endemic recombination arena in which long-term ecological coexistence, bipartite genome organization, mixed infections, and persistent vector circulation collectively create conditions favorable for diversification and evolutionary experimentation. Critically, they emphasize that this endemic regime does not represent stasis: the recurrent generation of recombinant and reassortant variants means that endemic systems are evolutionarily active arenas, not inert reservoirs. The distinction between ecological stability and evolutionary stasis is central to understanding why endemic begomoviruses may, under altered ecological conditions, shift position along the continuum toward emergence. The authors also outline why PHYVV and PepGMV have not transitioned to an invasive regime elsewhere: both display strong geographic structuring consistent with regional adaptation, are primarily associated with pepper cultivation systems that lack the international trade-mediated dissemination routes that benefit TYLCV, and their bipartite genome organization imposes a co-dispersal requirement for both DNA-A and DNA-B components, potentially constraining long-distance spread relative to monopartite viruses.

TYLCV exemplifies the opposite evolutionary trajectory. One of the most globally disseminated begomoviruses, it is associated with tomato yellow leaf curl disease, a viral disease complex with major impacts on tomato (Solanum lycopersicum) production worldwide. Phylogeographic analyses suggest a probable Middle Eastern origin followed by extensive global dissemination driven by agricultural trade, vector expansion, and intensive crop production systems. In Mexico, TYLCV was initially detected in symptomatic tomato plants from the Yucatán Peninsula and subsequently reported in Sinaloa during the 2005–2006 tomato-growing seasons; viral sequences from these outbreaks displayed high nucleotide identity with TYLCV isolates previously described from the Caribbean region and Florida, supporting recent introduction events linked to transregional viral movement. Successful establishment was likely favored by intensive tomato production, continuous availability of susceptible hosts, and efficient vector-mediated transmission by the Bemisia tabaci cryptic species complex. Following introduction, TYLCV populations may undergo additional adaptive processes associated with host resistance and management-driven selection: in Mediterranean systems, deployment of resistant tomato cultivars has been associated with shifts in begomovirus population structure and viral composition, and recent analyses of the tomato ty-5 resistance network suggest that host resistance mechanisms can shape TYLCV–host interactions at both molecular and epidemiological levels. In the Mexican context, García-Estrada and colleagues identified intensive insecticide use targeting the whitefly, continuous cropping schedules, and the incremental adoption of Ty-gene-carrying tomato hybrids as key drivers shaping viral epidemiology in Sinaloa and Sonora. Although studies directly quantifying TYLCV population shifts in response to resistant cultivar deployment in Mexico remain limited compared to the Mediterranean literature, the growing adoption of Ty-1, Ty-3, and ty-5 resistance genes in commercial hybrids across northern Mexican production regions constitutes a parallel selection context that warrants targeted molecular surveillance.

The connections between the endemic and invasive pathosystems are where the framework becomes most consequential. In northern Mexico, TYLCV has been identified in double and triple infections involving PHYVV and/or PepGMV within pepper-associated disease complexes, demonstrating that resident and introduced begomoviruses can occupy overlapping ecological and epidemiological niches. Such coexistence exposes viruses with contrasting evolutionary histories to the same host species, vector populations, surrounding vegetation, and agricultural practices, creating evolutionary interfaces that connect the endemic and invasive ends of the continuum. Mixed infections may modify transmission dynamics through interactions within shared hosts and vectors, while coinfection creates the potential for genomic exchange through recombination, one of the principal drivers of begomovirus diversification. The importance of these ecological interfaces is supported by high-throughput sequencing studies documenting the co-circulation of multiple begomovirus species and related genomic sequences in non-cultivated plants from northern-Pacific Mexico, where begomovirus-associated DNA signatures were found in more than 60 percent of sampled plants across multiple regions. Additional evidence from Colima identified a novel recombinant begomovirus, sida chlorotic leaf virus (SiChLV, B. sidaflavusfolii), in weeds belonging to the genera Sida and Malvastrum, while also detecting crop-associated begomoviruses infecting non-cultivated plants, supporting the interpretation that weeds may function simultaneously as reservoirs, incubators of viral diversity, and environments favoring recombination events capable of generating new viral variants. Comparative evidence from Côte d’Ivoire, where a nationwide survey of cassava agroecosystems identified 65 plant species functioning as alternative hosts for cassava mosaic begomoviruses, and from Saudi Arabia, where high-throughput sequencing revealed the co-circulation of TYLCV, watermelon chlorotic stunt virus, and tomato leaf curl Palampur virus within cucurbit production systems alongside the emergence of a novel TYLCV lineage, illustrates the broader global applicability of the contact-zone concept.

Current begomovirus surveillance strategies remain largely focused on symptomatic crop outbreaks and single-pathogen diagnostics, despite increasing evidence that begomovirus emergence is driven by broader ecological and evolutionary interactions involving vectors, weeds, intercrops, alternative hosts, agricultural intensification, and viral coexistence. The authors propose that surveillance must evolve from a reactive framework toward an eco-evolutionary approach integrating genomic, ecological, and landscape-level information capable of identifying the interfaces where endemic and invasive viral systems converge and diversify. Specific operational recommendations include sentinel plot sampling in pepper–tomato interface regions to monitor ecological overlap and early mixed-infection events; systematic collection of weeds and ruderal vegetation along agroecosystem edges, particularly in contact-zone areas; regular monitoring of whitefly populations with cryptic species identification using molecular markers such as mtCOI typing; whole-genome sequencing of samples from mixed infections to detect recombination events and characterize novel viral variants; temporal sampling across consecutive crop cycles to capture seasonal dynamics and multi-season evolutionary trends; application of recombination screening pipelines such as RDP5 and SimPlot as standard components of begomovirus genomic surveillance; and integration of crop calendars, host plant distribution maps, and vector abundance data into spatially explicit epidemiological risk models. Emerging sequencing technologies, including Oxford Nanopore approaches, may further strengthen surveillance capacity by enabling real-time characterization of mixed infections, recombinant variants, and invasive begomovirus population dynamics. The authors caution that the suggested sampling efforts and thresholds are illustrative operational starting points intended to guide implementation and prioritization, not validated universal thresholds, and should be calibrated to local epidemiological context. Taken together, the findings support interpreting begomovirus emergence as an eco-evolutionary continuum rather than a collection of isolated epidemiological categories. In regions such as Mexico, West Africa, and the Middle East, where crop diversity, whitefly pressure, weed reservoirs, and intensive agriculture converge, surveillance frameworks integrating evolutionary biology, genomics, and agroecosystem ecology may help identify where viral persistence is likely to occur, where invasive lineages may become established, and where recombination-associated risks should be prioritized. Such an approach may ultimately shift begomovirus management from reactive outbreak response toward more anticipatory and risk-informed disease surveillance strategies, anticipating the ecological conditions that favor viral emergence, diversification, and long-term persistence before outbreaks occur.

Subject of Research: An eco-evolutionary perspective on endemic persistence and invasive emergence of begomoviruses in Mexico

Article Title: An eco-evolutionary perspective on endemic persistence and invasive emergence of begomoviruses in Mexico

Article References: Aviña-Padilla, K., Alcántar-Aguirre, F. C., Zamora-Macorra, E. J., Vasquez-Gutierrez, U., Carrillo-Tripp, J., & Diaz-Lara, A. (2026). An eco-evolutionary perspective on endemic persistence and invasive emergence of begomoviruses in Mexico. Frontiers in Virology, 6, Article 1897263. https://doi.org/10.3389/fviro.2026.1897263

Image Credits: AI Generated

DOI: 10.3389/fviro.2026.1897263

Keywords: eco-evolutionary, perspective, endemic, persistence, invasive, emergence, begomoviruses, Mexico, scientific research