Plant Pathogen Invasion Modifies the Eco-Evolutionary Host Plant Interactions of an Endangered Checkerspot Butterfly

SIMPLE SUMMARY: Taylor’s checkerspot butterfly is a critically endangered species of northwestern North America that has become dependent on an exotic food plant, English plantain, which was acquired over a century ago. In the mid-2000s, a non-native plant pathogen from Europe, invaded Taylor’s checkerspot populations causing English plantain leaves to die in the winter when Taylor’s checkerspot larvae are feeding. We characterized butterfly and larval food plant (native and non-native) timing in Oregon and Washington populations and discovered that the invasive plant disease is active for ~60 days when larvae are feeding in January, February and March. Only one native larval foodplant, the annual Collinsia parviflora, can provide food for caterpillars during the time the plantain disease is common. However, this plant is rare in Taylor’s checkerspot habitat and may only be suitably timed to Washington checkerspot populations. Other native perennial larval food plants (Castilleja levisecta and likely C. hispida) do not appear suitably timed to provide resources throughout the entire Taylor’s checkerspot lifecycle in the low-elevation English plantain dependent populations. Understanding and accounting for the plant population disease dynamics is essential for the long-term conservation of Taylor’s checkerspot butterfly. ABSTRACT: New plant pathogen invasions typified by cryptic disease symptoms or those appearing sporadically in time and patchily in space, might go largely unnoticed and not taken seriously by ecologists. We present evidence that the recent invasion of Pyrenopeziza plantaginis (Dermateaceae) into the Pacific Northwest USA, which causes foliar necrosis in the fall and winter on Plantago lanceolata (plantain), the primary (non-native) foodplant for six of the eight extant Taylor’s checkerspot butterfly populations (Euphydryas editha taylori, endangered species), has altered eco-evolutionary foodplant interactions to a degree that threatens butterfly populations with extinction. Patterns of butterfly, larval food plant, and P. plantaginis disease development suggested the ancestral relationship was a two-foodplant system, with perennial Castilleja spp. supporting oviposition and pre-diapause larvae, and the annual Collinsia parviflora supporting post-diapause larvae. Plantain, in the absence of P. plantaginis disease, provided larval food resources throughout all butterfly life stages and may explain plantain’s initial adoption by Taylor’s checkerspot. However, in the presence of severe P. plantaginis disease, plantain-dependent butterfly populations experience a six-week period in the winter where post-diapause larvae lack essential plantain resources. Only C. parviflora, which is rare and competitively inferior under present habitat conditions, can fulfill the post-diapause larval feeding requirements in the presence of severe P. plantaginis disease. However, a germination timing experiment suggested C. parviflora to be suitably timed for only Washington Taylor’s checkerspot populations. The recent invasion by P. plantaginis appears to have rendered the ancestrally adaptive acquisition of plantain by Taylor’s checkerspot an unreliable, maladaptive foodplant interaction.