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

Abstract

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.

Are eastern and western monarch butterflies distinct populations? A review of evidence for ecological, phenotypic, and genetic differentiation and implications for conservation

“…Environmental contributions to migration‐associated traits may be particularly important for understanding differences observed between wild‐caught eastern and western monarchs, especially in light of studies showing that larval host plant species can influence adult monarch size (Decker, Soule, de Roode, & Hunter, 2019; Freedman, Jason, et al, 2020; Pocius et al, 2017). Environmental differences were also suggested as the reason for the significantly higher flight endurance of eastern compared to western monarchs (Talla et al, 2020).…”

“…This result is summarized in Table 1 (also reviewed in Pierce, Altizer, Chamerlain, Kronforst, & de Roode, 2015) and is robust to the kind and number of markers analyzed (i.e., microsatellites versus single nucleotide polymorphisms from whole genome sequencing) and consistent across studies. The most comprehensive study on the topic is from Talla et al (2020), who used whole genome resequencing for 14 eastern and 29 western monarchs and found no evidence for any genetic differentiation, including no fixed differences between east and west and no windows of elevated F ST in genome‐wide comparisons. While these studies are consistent with genetic panmixia between eastern and western monarchs, an alternative interpretation is recent divergence but with ongoing low levels of gene flow.…”

Further Insights on the Migration Biology of Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) from the Pacific Northwest

“…A large number (21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39) of individual citizen scientists in Oregon participated in this program annually, each rearing a varying number (3-600) of monarch butterflies in protected home gardens (~10% of rearers) or indoors during August-October. All captivereared monarchs were locally sourced from eggs or larvae found within Oregon, often in the back yard or property of the citizen, and were mostly reared in muslin cages on narrow-leaved milkweed (A. fascicularis Dcne.)…”

“…It is possible that western and eastern monarchs differ in their response to captive rearing. A recent study [30] showed that despite no genetic difference, eastern monarchs are capable of superior flight performance in the laboratory compared to western monarchs. It is also possible that the more modest migration of western compared to eastern monarchs may serve to mask any negative influences of captiverearing if they exist.…”

“…Combining the data from the two studies (n = 44) provides a mean daily rate of 25.0 km/day, lower than the 45.0 km/day reported by Brower et al [34] for migrating monarchs in the eastern US. Eastern US monarchs were shown to have superior flight performance than western monarchs [30], and most have a substantially longer distance (up to 4000 km) to travel to reach the overwintering area in Mexico. Monarchs in this study migrated from the PNW for distances of 465.1-1392.1 km to reach overwintering sites in California, similar to the shortest (486.0 km) and longest (1360.0 km) distances reported by James et al [13].…”