Genomic evidence for gene flow between monarchs with divergent migratory phenotypes and flight performance.

Monarch butterflies are known for their spectacular annual migration in eastern North America, with millions of monarchs flying up to 4,500 km to overwintering sites in central Mexico. Monarchs also live west of the Rocky Mountains, where they travel shorter distances to overwinter along the Pacific Coast. It is often assumed that eastern and western monarchs form distinct evolutionary units, but genomic studies to support this notion are lacking. We used a tethered flight mill to show that migratory eastern monarchs have greater flight performance than western monarchs, consistent with their greater migratory distances. However, analysing more than 20 million SNPs in 43 monarch genomes, we found no evidence for genomic differentiation between eastern and western monarchs. Genomic analysis also showed identical and low levels of genetic diversity, and demographic analyses indicated similar effective population sizes and ongoing gene flow between eastern and western monarchs. Gene expression analysis of a subset of candidate genes during active flight revealed differential gene expression related to nonmuscular motor activity. Our results demonstrate that eastern and western monarchs maintain migratory differences despite ongoing gene flow, and suggest that migratory differences between eastern and western monarchs are not driven by select major-effects alleles. Instead, variation in migratory distance and destination may be driven by environmentally induced differential gene expression or by many alleles of small effect.

Migratory monarchs wintering in California experience low infection risk compared to monarchs breeding year-round on non-native milkweed.

Long-distance migration can lower infection risk for animal populations by removing infected individuals during strenuous journeys, spatially separating susceptible age classes, or allowing migrants to periodically escape from contaminated habitats. Many seasonal migrations are changing due to human activities including climate change and habitat alteration. Moreover, for some migratory populations, sedentary behaviors are becoming more common as migrants abandon or shorten their journeys in response to supplemental feeding or warming temperatures. Exploring the consequences of reduced movement for host-parasite interactions is needed to predict future responses of animal pathogens to anthropogenic change. Monarch butterflies (Danaus plexippus) and their specialist protozoan parasite Ophryocystis elektroscirrha (OE) provide a model system for examining how long-distance migration affects infectious disease processes in a rapidly changing world. Annual monarch migration from eastern North America to Mexico is known to reduce protozoan infection prevalence, and more recent work suggests that monarchs that forego migration to breed year-round on non-native milkweeds in the southeastern and south central Unites States face extremely high risk of infection. Here, we examined the prevalence of OE infection from 2013 to 2016 in western North America, and compared monarchs exhibiting migratory behavior (overwintering annually along the California coast) with those that exhibit year-round breeding. Data from field collections and a joint citizen science program of Monarch Health and Monarch Alert showed that infection frequency was over nine times higher for monarchs sampled in gardens with year-round milkweed as compared to migratory monarchs sampled at overwintering sites. Results here underscore the importance of animal migrations for lowering infection risk and motivate future studies of pathogen transmission in migratory species affected by environmental change.