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.