The impact of habitat loss on molecular signatures of coevolution between an iconic butterfly (Alcon blue) and its host plant (Marsh gentian)

Habitat loss is threatening natural communities worldwide. Small and isolated populations suffer from inbreeding and genetic drift, which jeopardize their long-term survival and adaptive capacities. However, the consequences of habitat loss for reciprocal coevolutionary interactions remain poorly studied. In this study, we investigated the effects of decreasing habitat patch size and connectivity associated with habitat loss on molecular signatures of coevolution in the Alcon blue butterfly (Phengaris alcon) and its most limited host, the marsh gentian (Gentiana pneumonanthe). Because reciprocal coevolution is characterized by negative frequency-dependent selection as a particular type of balancing selection, we investigated how signatures of balancing selection vary along a gradient of patch size and connectivity, using single nucleotide polymorphisms (SNPs). We found that signatures of coevolution were unaffected by patch characteristics in the host plants. On the other hand, more pronounced signatures of coevolution were observed in both spatially isolated and in large Alcon populations, together with pronounced spatial variation in SNPs that are putatively involved in coevolution. These findings suggest that habitat loss can facilitate coevolution in large butterfly populations through limiting swamping of locally beneficial alleles by maladaptive ones. We also found that allelic richness (A(r)) of the coevolutionary SNPs is decoupled from neutral A(r) in the butterfly, indicating that habitat loss has different effects on coevolutionary as compared with neutral processes. We conclude that this specialized coevolutionary system requires particular conservation interventions aiming at generating a spatial mosaic of both connected and of isolated habitat to maintain coevolutionary dynamics.