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 kilometers 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, analyzing 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 non-muscular 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.

The ‘migratory connectivity’ concept, and its applicability to insect migrants

“…Further entomological radar [87], genetic [40,41,63,79], stable isotope [11,15,28,42] and individual marking [35,88] studies carried out in other regions and biomes of the world are needed to answer questions about the level of connectivity in insect migration systems. An exciting recent development is the reduction in weight of electronic tagging devices [89] which may help to get better flightpath data for very large insects (such as green darner dragonflies [65,67]), although it will take time to build up a database of migratory tracks (such as those emerging from decades of bird tagging).…”

“…This pattern is in stark contrast to the monarch butterfly, which notwithstanding its seemingly greater directional control, appears to experience a greater degree of population mixing across its entire summer range (Fig. 1) [40,41]. The level of detail known about the spatial population dynamics and migratory routes of the two noctuids described here is rather atypical for the family, and for most species we are unable to assess the level of migratory connectivity (albeit we predict it will be considerably lower or zero in most migrant noctuids); given the agricultural and economic significance of this group, this situation should be urgently addressed.…”

“…These recent observations of a much greater degree of mixing between eastern and western monarchs in Mexico suggest that migratory connectivity will be lower than previously believed. Indeed, molecular studies indicate that all North American monarchs constitute a single panmictic population that shows a lack of genetic divergence between eastern and western monarchs [40,41].…”

Butterfly Conservation in China: From Science to Action

“…Quantifying population structure would benefit determining how management strategies, population histories (via monitoring data), and/or environments influence patterns of diversity [ 118 , 119 , 120 , 121 , 122 , 123 , 124 , 125 , 126 ]. Also, identifying levels and directions of gene flow and the number of private alleles in populations can provide critical information for a more effective conservation strategy in terms of increasing fitness [ 121 , 127 , 128 , 129 , 130 , 131 , 132 ]. With the advance of high throughput sequencing and non-lethal sampling technologies [ 133 , 134 , 135 , 136 , 137 ], carrying out regular monitoring of the temporal shifts in the genetic diversity of focal species is actually a cost-effective and butterfly-friendly method to accumulate large volume of data for future conservation strategies.…”

Are Eastern and Western Monarch Butterflies Distinct Populations? A Review of Evidence for Ecological, Phenotypic, and Genetic Differentiation and Implications for Conservation

“…Eastern and western monarchs appear to harbor comparable levels of genetic diversity, as seen in measures of allelic richness using microsatellites (Pierce et al 2014), the r atio of heterozygote to homozygote genotypes (Zhan et al 2014), and various other measures (Talla et al 2020, Hemstrom et al in review). The lack of fixed genetic differences between eastern and western North America suggests that there are no strongly selected genetic variants that contribute to adaptation specifically to eastern or western North American environments (Talla et al 2020). Experiments that reciprocally translocate eastern and western monarchs and assess their ability to exhibit appropriate migration-associated behaviors (e.g.…”