Phytophagous insects constitute one of the most diverse groups of organisms, with over half a million described species. This extraordinary diversification is largely attributed to their close associations with host plants (Futuyma and Agrawal, 2009). The majority of phytophagous insects exhibit a high degree of specialization, typically feeding on a narrow range of plants within a single genus or family, and in some cases, even a single plant species (Forister et al., 2015). Such specialization is thought to drive reproductive isolation and, ultimately, speciation (Drès and Mallet, 2002; Peccoud et al., 2009). As a result, host-plant specialization is considered the norm, while generalist species (i.e. those capable of utilizing a wide range of host plants), are relatively rare.

The evolutionary success of specialists over generalists has been the focus of extensive research, though no single explanation fully accounts for this phenomenon. Instead, it likely results from a complex interplay of ecological, evolutionary, and physiological factors. One prominent explanation involves co-evolution between plants and herbivorous insects (Ehrlich and Raven, 1964). Over evolutionary timescales, plants develop defense mechanisms, while insects evolve corresponding counter-adaptations, leading to increasingly fine-tuned interactions that promote specialization (Edger et al., 2015). Additionally, genetic trade-offs in host use may further reinforce specialization, as adaptation to a specific host plant often comes at the cost of reduced performance on alternative hosts (Futuyma and Moreno, 1988; Forister et al., 2015).

Despite the prevalence of specialization, there are notable exceptions: generalist species that thrive on a wide range of host plants spanning multiple botanical families. Examples include the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae), which feeds on over 350 plant species across 76 families (Tay et al., 2023), the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae), with a host range exceeding 600 species from 74 families (De Barro et al., 2011), and the desert locust Schistocerca gregaria (Orthoptera: Acrididae), which consumes natural vegetation and a wide range of crops (Showler, 2002). The success of these generalists may stem from their broader tolerance for diverse environmental conditions, enhanced detoxification mechanisms, or flexible feeding behaviors. For instance, generalists usually have a range of detoxification enzymes that can neutralize many different plant chemicals, allowing them to feed on various plants without being harmed by their specific defenses (Govind et al., 2010; Simon et al., 2015). Genetic factors may also play a role in promoting generalism under certain conditions. Specialization often makes phytophagous insects highly dependent on the availability of their preferred host plants, which, in extreme cases, can lead to population declines or even extinction if those plants become scarce. Specialization is thus often associated with limited genetic diversity. In contrast, generalist species tend to maintain higher levels of genetic diversity, providing a broader foundation for natural selection to act upon. This genetic variability can enhance their capacity to adapt to new host plants and to fluctuating environmental conditions, increasing their resilience in unstable ecosystems such as agricultural landscapes (Hardy et al., 2020).

However, even among generalist species, differentiation can occur, leading to the formation of cryptic species complexes or host-associated populations. For instance, S. frugiperda comprises at least two genetically distinct strains: a corn strain and a rice strain. Despite being morphologically identical, these strains exhibit strong host plant preferences, with the corn strain primarily feeding on maize, sorghum, and cotton, while the rice strain specializes on rice and other grasses (Durand et al., 2022). Similarly, the pea aphid Acyrthosiphon pisum consists of at least 15 host-adapted biotypes, each specialized to feed on a restricted set of legume species (Peccoud et al., 2009, 2015). Furthermore, the host breadth of generalist insects is often assessed under controlled laboratory conditions, which may not fully capture the challenges they face in natural environments (Finlay-Doney and Walter, 2012). Factors such as predation, competition, and environmental variability can thus constrain their ability to exploit multiple hosts in the wild. As a result, truly generalist species may be even rarer than currently assumed.

The peach-potato aphid Myzus persicae has a very broad host range, encompassing more than 400 plant species, both cultivated and non-cultivated, belonging to more than 40 different botanical families (Blackman and Eastop, 2000; Bass et al., 2014). This species stands out from most other aphid species, which are typically specialized to feed on a limited number of host plants within the same plant family (Peccoud et al., 2010; Shih et al., 2023). The classification of M. persicae as a true generalist has been challenged in several studies, beginning with the identification of a tobacco-adapted form. Thus, certain populations that have specialized in feeding on tobacco exhibit distinct morphological and genetic differences from M. persicae sensu stricto (s.s.) and have been formally designated as M. persicae subsp. nicotianae (Blackman, 1987; Margaritopoulos et al., 2007). More recent genetic research, utilizing highly polymorphic markers or whole-genome sequencing, has revealed additional evidence of host-associated differentiation, with some genetic distinction observed among populations feeding on peach, pepper, and oilseed rape (Zamoum et al., 2005; Singh et al., 2021; Roy et al., 2022).

In the present study, we conducted an extensive sampling of M. persicae performed as part of a project aimed at identifying the sources of vectors and viruses responsible for the beet yellowing disease (Nio et al., 2025). Our main objective was to analyze the clonal diversity of M. persicae across different regions in northern France and on various host plants where this aphid can potentially overwinter. More specifically, we aimed to investigate whether M. persicae populations exhibited host-plant-based structuring and if so, to determine whether there is field evidence supporting the existence of clones capable of feeding on multiple plant species. By examining its genetic population structure and host-plant associations, this study was designed to assess whether M. persicae can truly be classified as a generalist.

Our study provides robust evidence that Myzus persicae populations in northern France are predominantly composed of a few highly successful superclones that exhibit remarkable ecological generalism. Contrary to the hypothesis that M. persicae might be composed of cryptic host-specialized lineages, we found no clear association between multilocus genotypes (MLGs) or genetic clusters and specific host plants, even across distantly related botanical families. These results reinforce the status of M. persicae as a true polyphagous (=generalist) species and underscore the ecological dominance of a small number of genotypes in natural populations of this aphid.

The high clonal structure observed, reflected by a low G:N ratio (0.14), the overwhelming representation of four superclones, and signs of a clonal diversification provides evidence that asexual reproduction plays a dominant role in shaping the population structure of M. persicae in the northern half of France. The predominance of asexual reproduction in this region is likely driven by the relatively mild winter climate, which permits parthenogenetic overwintering and consequently favours aphid genotypes that do not invest in the production of energetically costly sexual morphs (Rispe et al., 1998; Simon et al., 2002).

One particularly intriguing aspect of our results is the identification of Cluster 2, which differed markedly from other clusters. This group exhibited higher genetic diversity, longer branch lengths, and a positive inbreeding coefficient, all consistent with a history of sexual reproduction (Halkett et al., 2005). These genotypes were genetically distant from others, possibly representing rare recombinants produced during sexual cycles. Similar patterns of rare sexual recombination within largely asexual populations have been reported in previous works on aphids including M. persicae, Rhopalosiphum padi and Sitobion avenae (Haack et al., 2000; Delmotte et al., 2002; Vorburger et al., 2003a; Gilabert et al., 2009). This pattern is rare among the predominantly parthenogenetic populations of M. persicae in temperate zones and could reflect either recent loss of sex or immigration from regions where cyclical parthenogenesis – i.e. the alternation of asexual and sexual generations within a year – is more common because of harsher winters and more widespread primary hosts (Guillemaud et al., 2003; Roy et al., 2022).

Interestingly, the MLGs in Cluster 2 were not dominant in the population, suggesting that although sexual reproduction introduces novel genetic variation, these genotypes may not be as competitively successful under current field conditions as the well-established superclones. The fact that the four superclones were found consistently across multiple years, over large geographic areas, and on diverse host plants suggests they possess broad ecological plasticity. Their prevalence in suction and yellow traps further suggests that, in addition to their ability to exploit a broad spectrum of host plant species, they are also efficient dispersers, likely enhancing their capacity to dominate landscapes with mixed or shifting host-plant communities. Similar patterns have been observed in other aphid species where parthenogenesis allows for the rapid expansion of fit genotypes (Vorburger et al., 2003a; Gilabert et al., 2009; Figueroa et al., 2018).

While the dominance of a few clones might suggest potential bottlenecks or founder effects, our STRUCTURE and Neighbor-Joining analyses show that on the contrary the major superclones are genetically distinct and belong to separate clusters. This argues for the independent evolutionary origin of the MLGs concerned rather than clonal amplification from a single recent ancestor. The presence of multiple closely related MLGs within clusters, especially those with low allelic divergence and connected by short branches, supports the view of clonal diversification through stepwise mutations, a hallmark of long-term asexuality (Barraclough et al., 2003; Halkett et al., 2005; Tang et al., 2014). These clonal radiations likely represent microevolutionary processes driven by mutation accumulation in the absence of recombination (Delmotte et al., 2002; Barraclough et al., 2003). Clustering and genetic distance analyses identified an optimal partitioning into nine distinct clusters. Notably, if Cluster 2 is predominantly composed of cyclically parthenogenetic lineages (a hypothesis we could not firmly demonstrate, as we were unable to directly assess their reproductive phenotype), this suggests that the populations of M. persicae in northern France are primarily represented by eight main clonal lineages, each derived from independent ancestral origins followed by subsequent diversification. The precise origins, both temporal and geographical, of these independent clonal diversification events remain unclear and warrant further investigation through the integration of our dataset into a broader survey encompassing a wider geographical range.

Our findings provide important insights into the ecology of generalism in aphids. One might expect that exploitation of multiple host species would be achieved through a mosaic of specialized genotypes, but our results do not support this view. The absence of host-associated differentiation in the STRUCTURE analysis, and the lack of phylogenetic clustering by host plant in the genetic tree, provide strong evidence against the existence of cryptic host races within our sampled populations. This contrasts with previous studies on M. persicae that reported host-based population structure (Zamoum et al., 2005; Singh et al., 2021; Roy et al., 2022). However, much of the host-associated differentiation in those studies was driven by individuals collected from tobacco and peach, hosts that were not included in the present survey. Our results also contrast with findings in other aphids such as the pea aphid (Acyrthosiphon pisum) or the cotton-melon aphid (Aphis gossypii), where host-associated lineages show clear genetic structuring (Vanlerberghe-Masutti and Chavigny, 1998; Peccoud et al., 2009). Our results further demonstrate that broad host use is a property of individual clones of M. persicae, particularly the superclones, rather than a result of population-level polymorphism for host specialization. In herbivorous insects, generalist feeding strategies are often thought to be evolutionarily unstable due to trade-offs in host use and specialization (Futuyma and Moreno, 1988; Joshi and Thompson, 1995). However, M. persicae stands out as an exception, as do some other species that are partially or exclusively sexual, such as whiteflies, fall armyworms and desert locusts. Despite being a generalist species with over 400 recorded host plant species (Blackman and Eastop, 2000), our study confirms that M. persicae generalism is not merely a species-level trait but a property of individual superclones. These lineages, notably M1, M2, M7, and M10, were found on diverse hosts spanning ten botanical families and constituted more than half of all genotyped individuals. Two main hypotheses explain the persistence of parthenogenetic lineages. The frozen niche variation (FNV) hypothesis suggests these lineages consist of specialized genotypes, each adapted to a narrow niche, potentially outcompeting their more generalist sexual ancestors (Vrijenhoek, 1979; Vrijenhoek and Parker, 2009). In contrast, the general-purpose genotype (GPG) hypothesis proposes that parthenogenetic lineages have broadly adapted genotypes resulting from long term selection by environmental heterogeneity (Baker, 1965; Lynch, 1984). While both hypotheses have received empirical support (Vorburger et al., 2003b; Maraun et al., 2022; Godefroid et al., 2024), our results favor the GPG hypothesis, suggesting that generalist clones persist longer than specialist ones over evolutionary timescales.

Several traits may contribute to the broad host range observed in the M. persicae superclones. First, these clones may exhibit greater behavioral plasticity in host choice and acceptance, enabling flexible foraging strategies and enhancing their survival and reproduction. Second, they may possess specific metabolic or physiological adaptations that enable them to adjust to a wide variety of host plants. An experimental study involving a generalist M. persicae clone exposed to unrelated host plant species under controlled laboratory conditions revealed coordinated expression of gene clusters linked to host shift, notably including cathepsin B and cuticular protein genes (Mathers et al., 2017). These findings mean that transcriptional plasticity and epigenetic regulation play a key role in facilitating host plant acclimation in generalist (i.e. phytophagous) clones (Shih et al., 2023). Third, detoxification capacity plays a critical role in shaping host range by enabling herbivorous insects to neutralize or tolerate harmful plant compounds encountered during feeding (Simon et al., 2015; Shih et al., 2023). Interestingly, insecticide-resistant M. persicae genotypes have been shown to exhibit elevated expression of detoxifying enzymes such as cytochrome P450s, esterases, and glutathione S-transferases (Silva et al., 2012; Troczka et al., 2021; Bass and Nauen, 2023). In particular, a study on the tobacco-adapted race, which is tolerant to nicotine, revealed overexpression of a cytochrome P450 gene, CYP6CY3, driven by gene amplification and promoter alterations (Puinean et al., 2010; Bass et al., 2013). Subsequent research confirmed that these regulatory changes in CYP6CY3 expression were responsible for adaptation to tobacco, potentially contributing to race formation (Singh et al., 2020). Such genetic innovations likely involved transposable elements, which often accumulate near loci encoding xenobiotic metabolism genes (Baril et al., 2023). The four superclones identified in this study, along with many other multilocus genotypes (MLGs), are likely to carry multiple genes conferring insecticide resistance, consistent with recent findings in southern French populations of M. persicae (Roy et al., 2022). Characterizing the resistance mechanisms in these superclones and investigating their potential role in broad tolerance to plant defenses will doubtless provide valuable insights into the molecular basis of generalism and xenobiotic resistance. Together, these traits may explain the nutritional plasticity associated with M. persicae superclones.

Our work, which reveals the dominance of a few M. persicae clones with broad ecological tolerance, raises important concerns from a pest management perspective. While ecological theory suggests that specialization can confer fitness advantages under stable environmental conditions (Colles et al., 2009; Wang et al., 2019), our results indicate that in the highly dynamic context of conventional agriculture, generalist genotypes may have a selective advantage. Agricultural landscapes are generally characterized by frequent crop rotation, the use of mixed cultivars, and regular chemical applications, factors that create a constantly changing environment in which flexible and resilient genotypes are likely to thrive (Gilabert et al., 2009; Hardy et al., 2020). The M. persicae superclones capable of exploiting multiple host plants and dispersing over long distances are also likely to be those best equipped to resist insecticides and to transmit a broad array of phytopathogenic viruses (Bass et al., 2014; Nio et al., 2025). Continuous monitoring of the clonal composition of M. persicae in these landscapes is therefore strongly advocated, not only to understand ecological and evolutionary dynamics, but also in order to anticipate the spread of aphid-borne viruses and the emergence and dissemination of insecticide resistance (van Emden and Harrington, 2017).

In conclusion, our study supports the hypothesis that M. persicae is a true ecological generalist, with a population structure dominated by a small number of widespread and highly plastic superclones. These genotypes show no evidence of host-plant specialization and appear to thrive in diverse agricultural environments. Future research should focus on the molecular mechanisms underlying their ecological success and explore whether their dominance is maintained under different environmental pressures or pest control strategies.