Maintaining genetic diversity and population panmixia through dispersal and not gene flow in a holocyclic heteroecious aphid species

Abstract

Heteroecious holocyclic aphids exhibit both sexual and asexual reproduction and alternate among primary and secondary hosts. Most of these aphids can feed on several related hosts, and invasions to new habitats may limit the number of suitable hosts. For example, the aphid specialist Aphis glycines survives only on the primary host buckthorn (Rhamnus spp.) and the secondary host soybean (Glycine max) in North America where it is invasive. Owing to this specialization and sparse primary host distribution, host colonization events could be localized and involve founder effects, impacting genetic diversity, population structure and adaptation. We characterized changes in the genetic diversity and structure across time among A. glycines populations. Populations were sampled from secondary hosts twice in the same geographical location: once after secondary colonization (early season), and again immediately before primary host colonization (late season). We tested for evidence of founder effects and genetic isolation in early season populations, and whether or not late-season dispersal restored genetic diversity and reduced fragmentation. A total of 24 single-nucleotide polymorphisms and 6 microsatellites were used for population genetic statistics. We found significantly lower levels of genotypic diversity and more genetic isolation among early season collections, indicating secondary host colonization occurred locally and involved founder effects. Pairwise F ST decreased from 0.046 to 0.017 in early and late collections, respectively, and while genetic relatedness significantly decreased with geographical distance in early season collections, no spatial structure was observed in late-season collections. Thus, late-season dispersal counteracts the secondary host colonization through homogenization and increases genetic diversity before primary host colonization.

The Use of Refuge in Host Plant Resistance Systems for the Control of Virulent Biotype Adaptation in the Soybean Aphid (Hemiptera: Aphididae)

“…Soybean aphids migrate from soybean to Rhamnus in early autumn, where they sexually reproduce, admixing avirulence and virulence in the next generation. Though this movement has not been studied in detail, it is likely to mirror the movement of soybean aphid from Rhamnus to soybean, i.e., being characterized by local migration with strong bottlenecks (Bahlai et al 2010, Orantes et al 2012. Local migration by soybean aphid suggests that populations in the northern United States and southern Canada would have the greatest genetic input to the following generation, as Rhamnus species distribution is asymmetric with the greatest density in these regions (Heimpel et al 2010).…”

“…A regionally based IRM plan for Rag varieties may be most effective under these conditions. However, the soybean aphid rapidly disperses over large distances (Orantes et al 2012), and even aphids from distant Þelds may still be involved in sexual reproduction.…”

“…Furthermore, soybean aphids sexually reproduce on a separate host, reducing the probability that physical proximity of biotypes in soybean leads to random sexual admixture (Puterka andBurton 1991, Michel et al 2011). The soybean aphidÕs ability to disperse over large geographic areas (Orantes et al 2012) does suggest that sexual gene pools are likely indicative of average gene frequencies across soybean growing regions, but whether or not this translates to random mating on buckthorn is unknown. Considering these differences, the proliferation of virulence is primarily dependent on the relative asexual reproductive success of biotypes on soybean.…”

Geographic Distribution and Intrabiotypic Variability of Four Soybean Aphid Biotypes

“…Because both primary and secondary hosts are common and soybean aphids disperse extensively among them on an annual basis, there are few barriers to gene flow among soybean aphid populations, resulting in genetic homogenization across North America (Orantes et al, 2012). Because both primary and secondary hosts are common and soybean aphids disperse extensively among them on an annual basis, there are few barriers to gene flow among soybean aphid populations, resulting in genetic homogenization across North America (Orantes et al, 2012).…”

“…Because both primary and secondary hosts are common and soybean aphids disperse extensively among them on an annual basis, there are few barriers to gene flow among soybean aphid populations, resulting in genetic homogenization across North America (Orantes et al, 2012). Orantes et al (2012) and Wenger and Michel (2013) concluded that late-season aphid dispersal homogenizes the aphid population and increases genetic diversity before colonization of buckthorn, the primary host. They concluded that these patterns are consistent with expected biotypic virulence due to either nongenetic (possibly environmental) mechanisms or widely dispersed genetic mechanisms.…”