Connectivity and dispersal mode shape the landscape genetics of a carnivorous pitcher plant-arthropod metacommunity

Abstract

Dispersal differences between hosts and their symbionts can generate mismatched population structure, potentially destabilizing beneficial interactions across space. We tested this possibility in the carnivorous pitcher plant Darlingtonia californica and its obligate arthropod associates, the midge Metriocnemus edwardsi and the mite Sarraceniopus darlingtoniae, sampled across sites spanning the hosts patchy range in Oregon and northern California, USA. Comparing nuclear and chloroplast genomic data from D. californica with mitochondrial COI data from both arthropods, we tested how range position, landscape connectivity, and dispersal mode influence population genetic structure across this mutualistic metacommunity. Host plant populations supported the central-marginal hypothesis: nuclear diversity declined toward the range margins, and marginal populations showed greater nuclear genetic differentiation. Chloroplast variation was more weakly structured, most clearly separating the northern Oregon Coast populations and revealing cytonuclear discordance consistent with historical seed-mediated movement or chloroplast capture near the boundary between neighboring regions. Landscape connectivity estimated from an ecological niche model was also associated with genetic exchange. Circuit-theoretic current flow was positively related to effective migration inferred independently from plant genotypes. Further, landscape resistance explained variation in plant and mite differentiation beyond geographic distance alone. Both arthropods showed significant spatial congruence with the host plant but not with one another, a pattern inconsistent with co-dispersal and suggesting that each associate tracks the shared landscape according to its own dispersal biology. These results show that regional genetic concordance among obligate ecological partners can coexist with substantial differences in the processes governing their movement and local connectivity.