Introduction
Host adaptation is a key ecological characteristic of insect herbivores, influencing not only their survival and evolution but also the management strategies of them as agricultural pests (Forister et al. 2012; Simon and Peccoud 2018). Insect herbivores with broad host range (polyphagous) often comprise of host-specialized populations which perform much better on their natal hosts than on novel hosts. Ecologists have long been interested in insect host specialization that has been hypothesized to explain the extraordinary diversity of phytophagous insects in this globe (Braga et al. 2018). Genetic differentiation among host-specialized populations, if there was, implied the evolution of host races (or host biotypes or host strains) via host selection (StiremanIII et al. 2005), which were often used as evidences for the probability of ecological speciation (Drès and Mallet 2002; Peccoud et al. 2009).
The cotton-melon aphid, Aphis gossypii Glover, is extremely polyphagous, infesting more than 900 plant species in 116 plant families, such as Cucurbitaceae, Malvaceae, Solanaceae, Rutaceae and Asteraceae (Blackman and Eastop 2000). Like many other aphid species,A. gossypii has a complex life cycle, consisting of both holocyclic and anholocyclic life cycle. Previous studies reported that host-associated A. gossypii exhibited high fidelity to their natal host plants (Guldemond et al. 1994; Wool et al. 1995; Liu et al. 2002), which was highlighted in host exchange experiments between Malvaceae- and Cucurbitaceae-associated lineages (Liu et al. 2002; Liu et al. 2004; Najar-Rodríguez et al. 2009; Carletto et al. 2009; Satar et al. 2013). Besides fitness differences, studies detected genetic differentiations between host-associated populations of A. gossypii (Vanlerberghe-Masutti et al. 1998; Charaabi et al. 2008; Carletto et al. 2009; Wang et al. 2017), indicating evolution of host races in this aphid.
In severe winter areas, such as north China, A. gossypiifulfilled holocyclic life cycle, reproducing asexually on various secondary host plants and returning to woody host plants (usually hibiscus) once a year to lay cold resistant eggs (Blackman and Eastop 2000). In mild winter areas, such as Europe and Africa, A. gossypii maintained apomictic asexual reproduction constantly without annual return to overwintering hosts because parthenogenetic aphids could survive mild winter. Parthenogenetic aphids neither produced overwintering eggs nor survived cold winter on cucumber (Gilabert et al. 2009), and A. gossypii from hibiscus or cotton could not colonize cucumber (Liu et al. 2002; Najar-Rodríguez, et al. 2009). So, the origin of A. gossypii infesting cucumber remains elusive in severe winter areas. We conducted a two-year field observation in a garden which was planted with cucumber, cotton and hibiscus. Aphis gossypii infestation was not observed when the cucumber plants were young and healthy even though the adjacent cotton and hibiscus plants harbored large population of A. gossypii . However, aphid infestation was observed, generally starting from the lower leaves of cucumber that were infected with some phytopathogens. The aphids infesting cucumber were likely to come from hibiscus or cotton plants. Based on those observations, we proposed a hypothesis that host specialized aphid can adapt to new host plant under assistance of phytopathogen.
This study aimed to test the hypothesis about the life history ofA. gossypii infesting cucumber. Firstly, we tested host specialization of A. gossypii collected from hibiscus and cucumber from north China. Secondly, we chose a biotrophic phytopathogen to infect cucumber leaves, and compared the fitness of the hibiscus-specialized lineage on pre-infected and fresh cucumber leaves. Meanwhile, we monitored the piercing and sucking behaviors of the aphids on fresh and pre-infected cucumber. Finally, we compared the fitness of the hibiscus-specialized with feeding experience on pre-infested cucumber and the cucumber-specialized lineage on fresh cucumber. This study reveals a new pathway for insect adapting to new host plants and will provide new insights into host specialization.