Aphis gossypii Glover (Hemiptera: Aphididae) is a polyphagous pest renowned for causing substantial losses to both crop yields and quality across the globe (Morando et al., 2021). Additionally, non-crop plants (such as weeds) might contribute to the host transfer process of A. gossypii. These weeds, located within or adjacent to agricultural fields, can serve as alternative hosts, supporting the growth and reproduction of aphid populations (Caballero-López et al., 2011). And the secondary metabolites of different plants are different, and aphids that feed on different host plants for a long time may have population differentiation (Razmjou et al., 2010; Vorburger et al., 2017), thus increasing the biodiversity of farmland pests. However, there are several aspects remain elusive: the specific selection of plant hosts during aphid’s transfer from overwintering hosts to crops, the precise role of weeds in the aphid’s adaptation to host crops, and the underlying adaptive mechanisms that facilitate aphid’s transition between various hosts.

Microbial symbiosis is widely present in insects, with bacteria and insects co-evolving over hundreds of millions of years. This symbiotic relationship is vital for the survival and reproduction of insects. In the case of aphids, bacteria offer numerous benefits, including nutrition supply (Douglas et al., 2001; Rabatel et al., 2013) and protection from natural predators (Frago et al., 2017; Hrček et al., 2016). The symbiotic microorganisms harbored by aphids play a pivotal role in the process of host transfer. Typically, a shift in hosts alters the bacterial community structure within A. gossypii (Zhao et al., 2016). Furthermore, the bacterial symbionts present in aphids are influenced by the types of plants the aphids consume (Chandler et al., 2008). Notable differences exist in populations of Acyrthosiphon pisum on peach trees, Medicago sativa, and clover, and these variations are closely linked to their symbiotic microflora (Simon et al., 2003). Similarly, Aphis craccivora demonstrated distinct microbial communities when feeding on M. sativa and Robinia pseudoacacia, indicating a broad association between bacterial symbionts and host plants (Brady and White, 2013). Studies indicates that when the same aphid species feeds on different host plants, the prevalence of their symbionts often varies (Henry et al., 2015). Specifically, Hamiltonella was only detected in A. craccivora feeding on M. sativa, whereas Arsenophonus was exclusively present in A. craccivora feeding on R. pseudoacacia (Brady and White, 2013). However, there is a dearth of studies exploring the microbial changes of A. gossypii upon its transfer from cotton to alternative host plants. In consequence, it remains unclear how host adaptation alters the diversity of microbes within A. gossypii.

Solanum nigrum (Solanales: Solanaceae) is an annual broadleaf weed that grows rapidly in the field, distinguished by its vigorous growth, high fecundity, brief growth cycle, and persistent fruitfulness (Zhao et al., 2017). When fully mature, S. nigrum can occupy significant space, impeding light penetration and competing for nutrients with crops. These competitions lead to slower growth of crops, ultimately reducing both yield and quality. S. nigrum serves as an alternative host for aphids, especially in environments where cultivated crops are temporarily unavailable. Therefore, A. gossypii (Perng, 2002), Myzus persicae (Almohamad et al., 2006), Aulacorthum solani (Milbrath and Biazzo, 2012) and Brevicoryne brassicae (Coutts et al., 2006) often utilize S. nigrum as a host for growth and reproduction. In addition, S. nigrum stands as a important weed in corn and soybean fields (Dalley et al., 2004), with the potential to be parasitized by aphids. This host adaptability can pose a threat to crops, yields and ultimately food security. Nevertheless, the mechanisms by which A. gossypii adapts to S. nigrum, as well as the subsequent effects on its population expansion capacity upon returning to the original host crop, remains undefined.

Numerous studies have investigated the adaptability of A. gossypii to various host plants and the alterations in their internal microorganisms. However, the shifts in the symbiotic bacterial community of A. gossypii following host transfer, as well as their adaptive mechanism to plant hosts during this transition is not clear. Therefore, this paper initially constructed a life table for multi-generational growth of A. gossypii on S. nigrum, thereby assessing its adaptability to this host. Subsequently, utilizing 16S rRNA sequencing technology, we analyzed the dynamics of symbiotic microbial communities during A. gossypii adaptation to S. nigrum.

The results of this study offer insights into the adaptive mechanism of A. gossypii to the weed host S. nigrum, which is instrumental in unveiling its broader adaptive strategies following host transfers. Ultimately, this research provides theoretical guidance for the scientific prevention and control of A. gossypii.

Although A. gossypii is hosted by numerous plants, research on the role of weeds in its host shift remains limited. S. nigrum stands as a prominent weed in agricultural fields. Nevertheless, the adaptability mechanism of A. gossypii to S. nigrum, and the subsequent effects on its population expansion capacity upon returning to original host crop, are still not fully understood. S. nigrum serves as an alternative host for A. gossypii, particularly in environments where cultivated crops are temporarily unavailable. Our research emphasizes the multi-generational adaptation of S. nigrum and its role in enhancing the reproduction rates of A. gossypii. This adaptation of the weed may increase habitat suitability for the aphid, thereby facilitating its population growth. Elevated aphid populations can significantly impact crop yields through direct feeding damage (Ramalho et al., 2012) and the transmission of plant viruses (Smith and Chuang, 2014). In regions such as the North China Plain, where crops like cotton, corn, and vegetables are essential, the increased reproduction of A. gossypii could result in considerable economic losses (Zhang et al., 2018). A. gossypii can diminish plant vigor, stunt growth, and reduce both the quality and quantity of agricultural produce (Zhong et al., 2022), directly affecting farmers’ livelihoods and regional food supplies.

Host adaptation is a long process. The research revealed that no significant difference in r between A. gossypii initially reared on Hibiscus syriacus and those on Cucumis sativus after three generations (Zheng et al., 2007). When Tetranychus viennensis transfers from apple trees to other fruit trees, the first generation experiences negative effects on life table parameters, but these effects dissipate in succeeding generation (Li et al., 2006). A. gossypii develops faster on the original host compared to non-original host, and its r is higher on the original host (Satar et al., 2013), indicating inhibited development on the non-original hosts. Transferring A. gossypii from cotton to C. sativus and Abelmoschus manihot for four consecutive generations did not enhance its development (Satar et al., 2013). The first-generation life table parameters of Amphitetranychus viennensis suffered when transferred from Prunus serotine, which is conducive to its growth, to Malus domestica (Kafil et al., 2007). Likewise, when A. viennensis was transferred to Prunus avium, its first-generation life table parameters fared better than the third generation, showing no gradual adaptation to P. avium (Kafil et al., 2007). However, the difference of life table of a pest on different host crops may be caused by the difference of secondary metabolites (Abdelsalam et al., 2016), more experiments are essential to uncover the exact mechanism.

Our results demonstrated that A. gossypii gradually adapted to S. nigrum, with T5 demonstrating significant progress. The shape of l_x and m_x curves illustrate the interplay of life history traits and determine r, a common indicator for evaluating the adaptability of pest to plants (Bethke et al., 1998; Sandström and Pettersson, 1994). A later decline in the l_x curve and higher peak in the m_x indicate a the greater r and, consequently, higher aphid population growth potential. The r of A. gossypii on S. nigrum peaked at T5, signifying the highest population growth potential for this generation on S. nigrum. In the absence of alternative crops like G. hirsutum, A. gossypii can rapidly multiply on S. nigrum, maintaining a dense population.

Microbial symbionts play a pivotal role in enhancing the adaptability of pests to their hosts. In this study, significant changes were observed in the bacterial community of T5 and T10 of A. gossypii feeding on S. nigrum. At the phylum level, the abundance and species of bacterial communities remained stable across all groups, and the highest abundance of bacteria was Proteobacteria. Proteobacteria are recognized as a vital component of the intestinal flora in numerous herbivorous insects and fostering a beneficial symbiotic relationship with their hosts (Show et al., 2022). These insects provide a stable environment for Proteobacteria, which, in turn, endow their hosts with novel metabolic capabilities (Latorre et al., 2003).

Buchnera is a member of the Proteobacteria, which is the dominant bacterium in aphids growing on various host plants (Ma et al., 2021). Its roles extend to DNA replication, transcription, protein translation, secretion, energy metabolism, and amino acid biosynthesis for aphids (Baumann et al., 1995; Richards et al., 2010; Tian et al., 2023). In our study, a notable increase in the relative abundance of Buchnera was observed in T5 and T10, while no significant alteration was detected in the M and T1. Similarly, Buchnera content was significantly higher in A. gossypii reared on C. sativus for over 10 years compared to those on cotton (Zhang et al., 2016). The relative abundance of Buchnera in A. gossypii reared on Cucurbita pepo was also significantly higher than those on cotton (Xu et al., 2023). Collectively, the elevated abundance of Buchnera is related to the adaptation of A. gossypii to new host plants.

Arsenophonus (Proteobacteria) is an intracellular symbiotic bacteria of insects, generally belonging to the secondary symbiotic bacteria, which has a wide range of hosts and rich biodiversity (Chen et al., 2014). This bacterium plays a crucial part in enhancing the growth performance of aphids during amino acid deficiency (Tian et al., 2023; Wang et al., 2024). Furthermore, it mitigates the harmful effects of parasitic wasps to aphids (Heidari Latibari et al., 2023) and mediates host specialization of aphids (Tian et al., 2019). Notably, Arsenophonus is also the dominant bacteria in A. gossypii (Xu et al., 2020; Zhang et al., 2021). In our study, the relative abundance of Arsenophonus was significantly lower in T5 and T10 compared to M and T1. This finding suggests a decline in Arsenophonus as A. gossypii adapts to S. nigrum. Similar study has showed that a reduction in Arsenophonus abundance of plutella xylostella after treatment with the insecticide sulfoxaflor (Shang et al., 2021).

Based on the changes in the abundance of symbiotic bacteria and predictions from the KEGG function database, Buchnera and Arsenophonus may regulated metabolic processes, enabling A. gossypii to gradually adapt to the S. nigrum. Across various life stages of Adelphocoris suturalis, the function of symbiotic bacteria predominantly focuses on metabolic pathway (Xue et al., 2021). The signal transduction function of intestinal bacteria increased after 17 generations of P. xylostella shifted from Raphanus sativus to Amygdalus persica (Yang et al., 2020). In comparison to the findings of this study, KEGG function prediction analysis suggests that Buchnera and Arsenophonus contribute to the adaptation of A. gossypii to S. nigrum by engaging in metabolic functions, particularly in “carbohydrate metabolism,” “membrane transport,” “metabolism of cofactors and vitamins,” “energy metabolism,” and so on. To gain a comprehensive understanding of these disparities, further investigation is necessary, possibly including metagenomic analyses to explore the functional significance of these symbiotic bacteria and to unravel the causal relationships.

In this study, the growth and reproduction parameters of A. gossypii demonstrated a gradual adaptation process as its generations progressed on S. nigrum. Notably, the T5 generation of A. gossypii exhibited the highest level of adaptation to S. nigrum. Upon transferring A. gossypii, which had been domesticated by S. nigrum, back to G. hirsutum, T5-M displayed the greatest values for r, λ, and fecundity. Furthermore, significant changes were observed in the symbiotic bacteria of A. gossypii after several generations on S. nigrum compared to those on G. hirsutum. The abundance of Buchnera in T5 and T10 of A. gossypii reared on S. nigrum increased significantly, whereas the abundance of Arsenophonus decreased significantly.

The adaptability of A. gossypii to transition between distinct host species, for instance, from S. nigrum to G. hirsutum, underscores the intricate interactions within agricultural ecosystems. These interactions can impact biodiversity and crop yields, as the presence of adaptable pests like A. gossypii has the potential to exacerbate pest infestation on economically crucial crops such as cotton, corn or soybean. By comprehending the mechanisms of host adaptation and the symbiotic relationships involved, more effective strategies could be devised to reduce the negative influence of A. gossypii on food production.

In conclusion, this article unveils the consequences of adaptation of A. gossypii to S. nigrum on their capacity for population growth and the abundance of dominant bacteria, while clarifying the function of S. nigrum in the host transition process of A. gossypii. The findings of this study offer valuable insights for the development of an innovative control technology system targeting A. gossypii, as well as advancing scientific and comprehensive methods for managing pests and weeds in fields.