Cryptic Plutella species show deep divergence despite the capacity to hybridize

Abstract

BackgroundUnderstanding genomic and phenotypic diversity among cryptic pest taxa has important implications for the management of pests and diseases. The diamondback moth, Plutella xylostella L., has been intensively studied due to its ability to evolve insecticide resistance and status as the world’s most destructive pest of brassicaceous crops. The surprise discovery of a cryptic species endemic to Australia, Plutella australiana Landry & Hebert, raised questions regarding the distribution, ecological traits and pest status of the two species, the capacity for gene flow and whether specific management was required. Here, we collected Plutella from wild and cultivated brassicaceous plants from 75 locations throughout Australia and screened 1447 individuals to identify mtDNA lineages and Wolbachia infections. We genotyped genome-wide SNP markers using RADseq in coexisting populations of each species. In addition, we assessed reproductive compatibility in crossing experiments and insecticide susceptibility phenotypes using bioassays.ResultsThe two Plutella species coexisted on wild brassicas and canola crops, but only 10% of Plutella individuals were P. australiana. This species was not found on commercial Brassica vegetable crops, which are routinely sprayed with insecticides. Bioassays found that P. australiana was 19-306 fold more susceptible to four commonly-used insecticides than P. xylostella. Laboratory crosses revealed that reproductive isolation was incomplete but directionally asymmetric between the species. However, genome-wide nuclear SNPs revealed striking differences in genetic diversity and strong population structure between coexisting wild populations of each species. Nuclear diversity was 1.5-fold higher in P. australiana, yet both species showed limited variation in mtDNA. Infection with a single Wolbachia subgroup B strain was fixed in P. australiana, suggesting that a selective sweep contributed to low mtDNA diversity, while a subgroup A strain infected just 1.5% of P. xylostella.ConclusionsDespite sympatric distributions and the capacity to hybridize, strong genomic and phenotypic divergence exists between these Plutella species that is consistent with contrasting colonization histories and reproductive isolation after secondary contact. Although P. australiana is a potential pest of brassicaceous crops, it is of secondary importance to P. xylostella.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1183-4) contains supplementary material, which is available to authorized users.

Assessing genomic admixture between cryptic Plutella moth species following secondary contact

“…A better understanding of migration or transport routes enabling P. xylostella to colonize the world would help explain why this is the case. Several studies have found Australian P. xylostella mtDNA genomes have very low levels of diversity (Juric, et al 2016;Perry, et al 2018;Saw, et al 2006), which is indicative of a population bottleneck (and other factors), while we found…”

“…The fortuitous identification of Plutella australiana was unexpected and raised initial concern over its pest status and whether specific management practices were required. P. australiana populations collected from across southern Australia (Perry, et al 2018) and Australian P. xylostella (Endersby, et al 2006) lack genetic structure, showing these species are highly mobile. Adaptive introgression of advantageous traits from one of these species into the other could potentially spread across the Australian continent.…”

“…Genomic DNA purification was performed using phenol extractions, treated with RNaseA, precipitated with ethanol and resuspended in TE buffer (10 mM Tris, 0.1 mM EDTA). Species identification was performed using a PCR-RFLP diagnostic assay of the mitochondrial COI gene (Perry, et al 2018). Genome sequencing was performed using the Illumina HiSeq2500 or NextSeq platforms at the Australian Genome Research Facility and the Australian Cancer Research Facility.…”

“…Insecticide susceptibility appears to limit P. australiana's pest potential among cultivated brassica crops, however, introgression of insecticide resistance loci from P. xylostella could have serious consequences for agriculture. Plutella xylostella and P. australiana can hybridize in experimental laboratory crosses, despite their contrasting infection rates of endosymbiotic Wolbachia (Perry, et al 2018;Ward and Baxter 2017), which are known to cause reproductive incompatibility in some cases (Duplouy, et al 2013;Sasaki and Ishikawa 2000). Wolbachia infection is fixed among P. australiana yet extremely low in Australian P. xylostella (1.5%).…”

“…Wolbachia infection is fixed among P. australiana yet extremely low in Australian P. xylostella (1.5%). Although the strength of reproductive barriers in the field is unknown, limited numbers of SNP markers widely dispersed across the nuclear genome previously identified genetic structure between sympatric populations of P. xylostella and P. australiana (Perry, et al 2018). Due to P. australiana's apparent endemism and the relatively recent invasion of P. xylostella into Australia, we assessed the capacity for sympatric Australian Plutella species to exchange beneficial traits through disassortative mating and introgression in the field through analyzing whole genomes.…”