Parasite local adaptation has been a major focus of (co)evolutionary research on host-parasite interactions. Studies of wild host-parasite systems frequently find that parasites paired with local, sympatric host genotypes perform better than parasites paired with allopatric host genotypes. In contrast, there are few such tests in biological control systems to establish whether biological control parasites commonly perform better on sympatric pest genotypes. This knowledge gap prevents the optimal design of biological control programs: strong local adaptation could argue for the use of sympatric parasites to achieve consistent pest control. To address this gap, we tested for local adaptation of the biological control bacterium Pasteuria penetrans to the root-knot nematode Meloidogyne arenaria, a global threat to a wide range of crops. We measured the probability and intensity of P. penetrans infection on sympatric and allopatric M. arenaria over the course of four years. Our design accounted for variation in adaptation across scales by conducting tests within and across fields, and we isolated the signature of parasite adaptation by comparing parasites collected over the course of the growing season. Our results are largely inconsistent with local adaptation of P. penetrans to M. arenaria: in three of four years, parasites performed similarly well in sympatric and allopatric combinations. In one year, however, infection probability was 28% higher for parasites paired with hosts from their sympatric plot, relative to parasites paired with hosts from other plots within the same field. These mixed results argue for population genetic data to characterize the scale of gene flow and genetic divergence in this system. Overall, our findings do not provide strong support for using P. penetrans from local fields to enhance biological control of Meloidogyne.

To test for local adaptation of P. penetrans, we collected paired samples of M. arenaria and P. penetrans from six sites each year. Because the strength of local adaptation can vary with spatial scale, we collected samples from six plots within a single field in 2019 and 2020 and from six fields in 2021 and 2022. Each year, we compared the performance of P. penetrans when paired with sympatric and allopatric M. arenaria by measuring proxies for infection probability (attachment rate) and intensity (attachment load). In 2019 and 2020, we isolated the signature of parasite adaptation by comparing local adaptation of early-, mid-, and late-season parasites.