Unexpected diversity in historical biological control programs: Population genetics of the nematode Deladenus siricidicola in Australia and New Zealand

[Display omitted] •Australian and New Zealand D. siricidicola populations have unexpectedly high genetic diversity.•A novel lineage of D. siricidicola is dominant in Australia.•New Zealand and North American nematode populations share a common origin.•Genetic patterns may reflect original introductions and selection over biocontrol releases.•Newly found D. siricidicola diversity may improve biological control programs globally. The nematode Deladenus siricidicola is used for the biocontrol of the invasive woodwasp, Sirex noctilio, that infests Pinus globally. In New Zealand, D. siricidicola was accidentally introduced along with S. noctilio, after which its potential for biological control was realized in the 1960s. Additional strains of the nematode were collected from across its Eurasian distribution for the development of a biological control program in Australia in the 1970s. A strain from Hungary (Sopron) was originally selected for large-scale releases and later replaced by a strain that was collected from previously released populations in Tasmania (Kamona). The Kamona strain is still used today in biological control programs in Australia, South Africa and South America. Despite the long history of biocontrol, the nematode’s genetic diversity has not been studied in Australia and New Zealand. We assessed the population genetic diversity and structure of D. siricidicola in these countries using mitochondrial COI sequence data and 12 microsatellite markers. We also compared our data to that of a recent global diversity study. The results show a higher than expected diversity of the nematode in these Australasian countries, especially Australia. Three lineages previously defined from North America (A), Southern Hemisphere (B) and Spain (C) were identified in Australia (A, B, C) and New Zealand (A, B). A previously undescribed lineage (D), was identified in both Australia and New Zealand. Despite the evidence of admixture with other lineages, including the widely distributed biocontrol lineage (B; Kamona), lineage D remained distinguishable and dominant in these populations, even where Kamona has been released intensively for decades. Surprisingly, the results also revealed a shared history between populations in New Zealand and North America. These findings highlight the importance of understanding and monitoring genetic diversity in biological control programs and hold opportunities to improve both the selection and deployment of this nematode for the