Host‐associated differentiation in a highly polyphagous, sexually reproducing insect herbivore

Abstract

Insect herbivores may undergo genetic divergence on their host plants through host-associated differentiation (HAD). Much of what we know about HAD involves insect species with narrow host ranges (i.e., specialists) that spend part or all their life cycle inside their hosts, and/or reproduce asexually (e.g., parthenogenetic insects), all of which are thought to facilitate HAD. However, sexually reproducing polyphagous insects can also exhibit HAD. Few sexually reproducing insects have been tested for HAD, and when they have insects from only a handful of potential host-plant populations have been tested, making it difficult to predict how common HAD is when one considers the entire species’ host range. This question is particularly relevant when considering insect pests, as host-associated populations may differ in traits relevant to their control. Here, we tested for HAD in a cotton (Gossypium hirsutum) pest, the cotton fleahopper (CFH) (Pseudatomoscelis seriatus), a sexually reproducing, highly polyphagous hemipteran insect. A previous study detected one incidence of HAD among three of its host plants. We used Amplified fragment length polymorphism (AFLP) markers to assess HAD in CFH collected from an expanded array of 13 host-plant species belonging to seven families. Overall, four genetically distinct populations were found. One genetically distinct genotype was exclusively associated with one of the host-plant species while the other three were observed across more than one host-plant species. The relatively low degree of HAD in CFH compared to the pea aphid, another hemipteran insect, stresses the likely importance of sexual recombination as a factor increasing the likelihood of HAD.

Genome‐wide markers reveal temporal instability of local population genetic structure in the cotton fleahopper, Pseudatomoscelis seriatus (Hemiptera: Miridae)

“…Ultimately, our results indicate that woolly croton acts as a site of year‐end admixture for insects that have previously utilized other hosts including cotton during the growing season, at least in areas where it occurs. These findings were consistent with the results of previous studies that have found that individuals utilizing cotton in areas where woolly croton occurs were not genetically differentiated from those utilizing woolly croton during the growing season . Barman et al .…”

“…found a pattern of HAD in association with scurvy mallow, Malvella lepidota (Malvales: Malvaceae), and called into question the HAD described by Barman et al . by showing that those genotypes associated with horsemint also utilized other alternative wild hosts . Both of these previous studies examined relatively large geographic areas spanning multiple cotton‐growing regions, but sampled each study site only once.…”

A Genomic Perspective on the Generation and Maintenance of Genetic Diversity in Herbivorous Insects

“…Phylogenetic analyses reveal that while specialist insects evolve from generalists, generalists also frequently evolve from specialists (Janz and Nylin 2008). And population genomic approaches have revealed a range of host-associated differentiation, sometimes including the absence of host-associated differentiation, in polyphagous insect species (Antwi et al 2015). Overall, while host- or habitat-driven adaptation likely drives divergence among sympatric populations in some cases (Berlocher et al 2002; Feder et al 2013), a classic population genetic prediction remains relevant: when migration is frequent, the homogenizing effects of gene flow generally prevent divergence among populations (Yeaman and Otto 2011).…”

Habitat or temporal isolation: Unraveling herbivore–parasitoid speciation patterns using double digest RADseq

“…HAD has been recorded in diverse insect families across multiple orders (Antwi, Sword, & Medina, ; Ferrari, West, Via, & Godfray, ; Leppanen, Malm, Varri, & Nyman, ; Sword, Joern, & Senior, ), further suggesting that it is an important driver of speciation that contributed to the insect biodiversity we see today. In addition, HAD can have rippling effects at higher trophic levels, resulting in divergence of parasitoids in the form of cascading/sequential HAD (Abrahamson & Weis, ; Forbes, Powell, Stelinski, Smith, & Feder, ; Hood et al., ; Nicholls, Schönrogge, Preuss, & Stone, ; Stireman, Nason, Heard, & Seehawer, ).…”

“…As many parasitoids are also cryptic specialists that are tightly linked to the phenology of their hosts, cascading HAD on species lineages of herbivores could result in the sequential radiation of these hyperdiverse lineages of parasitoids (Forbes et al., ; Hood et al., ; Stireman et al., ). However, many previous studies of HAD and sequential HAD were limited to few molecular markers (Antwi et al., ; Hood et al., ; Leppanen et al., ; Nicholls et al., ; Stireman et al., ), which provides limited molecular characters to examine fine‐scaled species‐level differentiation. In addition, most studies focus on specialist herbivores with few studies on parasitoids.…”