Population genetics of a recent range expansion and subsequent loss of migration in monarch butterflies

Abstract

Range expansions—whether permanent or transient—strongly influence the distribution of genetic variation in space. Monarch butterflies are best known for long‐distance seasonal migration within North America but are also established as nonmigratory populations around the world, including on Pacific Islands. Previous research has highlighted stepwise expansion across the Pacific, though questions remain about expansion timing and the population genetic consequences of migration loss. Here, we present reduced‐representation sequencing data for 275 monarchs from North America (n = 85), 12 Pacific Islands (n = 136) and three locations in Australia (n = 54), with the goal of understanding (i) how the monarch's Pacific expansion has shaped patterns of population genetic variation and (ii) how loss of migration has influenced spatial patterns of differentiation. We find support for previously described stepwise dispersal across the Pacific and document an additional expansion from Hawaii into the Mariana Islands. Nonmigratory monarchs within the Mariana Islands show strong patterns of differentiation, despite their proximity; by contrast, migratory North American samples form a single genetically panmictic population across the continent. Estimates of Pacific establishment timing are highly uncertain (~100–1,000,000 years ago) but overlap with historical records that indicate a recent expansion. Our data support (i) a recent expansion across the Pacific whose timing overlaps with available historical records of establishment and (ii) a strong role for seasonal migration in determining patterns of spatial genetic variation. Our results are noteworthy because they demonstrate how the evolution of partial migration can drive population differentiation over contemporary timescales.

Population-specific patterns of toxin sequestration in monarch butterflies from around the world

“…Thus, we can only compare wild-caught butterflies from each island, which does not allow for us to formally disentangle genetic from environmental sources of variation in sequestered cardenolides. However, we feel fairly confident attributing any observed differences in wing cardenolide concentrations to genetic differences between islands for the following reasons: (1) all monarchs from Guam and Rota appear to have developed on the same host, A. curassavica (Figure S2); (2) in our greenhouse rearing experiment, plant cardenolide concentrations in A. curassavica did not positively correlate with butterfly wing concentrations (Figure S7), suggesting that any observed differences in wild-caught butterflies are unlikely to be driven by variation in host plants; (3) despite their proximity, monarchs from Guam and Rota show strong genome-wide patterns of differentiation (Hemstrom et al 2022), highlighting the potential for phenotypic divergence.…”

Considerable genetic diversity and structure despite narrow endemism and limited ecological specialization in the Hayden's ringlet, Coenonympha haydenii

“…In contrast, both migratory monarchs ( Danaeus plexippus ) and non‐migratory Heliconius sp. showed comparatively high nucleotide diversity ( π = 0.01–0.06 and 0.020–0.28, respectively) (Hemstrom et al., 2022; Kryvokhyzha, 2014; Martin et al., 2016; Talla et al., 2020). Migratory butterfly species have been shown to harbour higher levels of genetic diversity than non‐migratory species in general, possibly due to greater population sizes and connectivity (García‐Berro et al., 2023), so the substantial difference in nucleotide diversity between monarchs and Hayden's ringlets is not unexpected.…”

“…Patterns of genetic structure, or the organization of genetic diversity across geographic space, can help reveal contemporary gene flow and migratory routes (e.g. Gompert et al., 2021; Hemstrom et al., 2022), ecological specialization (e.g. Chaturvedi et al., 2018; Ferrari et al., 2012; Michell et al., 2023; Nosil et al., 2008), patterns of admixture (e.g.…”

Boundary effects cause false signals of range expansions in population genomic data

“…Previous simulation work has shown clines in ψ to be more sensitive and robust to detecting signatures of REs and estimating their origins compared to methods based on clines in genetic diversity (Peter andSlatkin 2015, 2013), where the expansion origin is expected to be the location with the strongest positive correlation between geographic distance and ψ. This approach has been increasingly applied in recent population genetic studies as it only requires one diploid individual to be sampled per population (Zhan et al 2014;Maisano Delser et al 2019;Prior et al 2020;Fifer et al 2022;Hemstrom et al 2022;Lesturgie et al 2023;Singhal, Wrath, and Rabosky 2022;Walsh et al 2022;Ioannidis et al 2021;He, Prado, and Knowles 2017;Jaya et al 2022). A further potential benefit of the methodology introduced in Peter andSlatkin (2013, 2015) is the use of the Time Difference of Arrival (TDoA) -a ranging technique regularly used in the Global Positioning System (GPS) that allows for the inference of range expansion origins also from unsampled geographic regions.…”