Modular switches shift monarch butterfly migratory flight behavior at their Mexican overwintering sites

Abstract

Eastern North American migratory monarch butterflies exhibit migratory behavioral states in fall and spring characterized by sun-dependent oriented flight. However, it is unclear how monarchs transition between these behavioral states at their overwintering site. Using a modified Mouritsen-Frost flight simulator, we confirm individual directionality and compass-based orientation (leading to group orientation) in fall migrants, and also uncover sustained flight propensity and direction-based flight reinforcement as distinctly migratory behavioral traits. By testing monarchs at their Mexican overwintering sites, we show that overwintering monarchs show reduced propensity for sustained flight and lose individual directionality, leading to the loss of group-level orientation. Overwintering fliers orient axially in a time-of-day dependent manner, which may indicate local versus long-distance directional heading. These results support a model of migratory flight behavior in which modular, state-dependent switches for flight propensity and orientation control are highly dynamic and are controlled in season- and location-dependent manners.

Keywords: Ecology; Entomology; Evolutionary biology.

Graphical abstract

Figure 1

A modified Mouritsen-Frost flight simulator captures essential features of migratory flight (A) Monarch butterfly flying in the modified simulator. We determined individual direction by training a model to identify the “origin” of the simulator (yellow box) and the head of the monarch (red box). The white box indicates a monarch identified in the model. (B) Directionality as measured by weighted r for summer non-migrants, fall migrants, and overwintering migrants. Error bars indicate 1.5 times interquartile range. (C–E) Orientation plots for all individuals tested in sunny conditions. Individual butterflies are represented by circles colored by membership score based on weighted r. The distance from the origin is given by individual r. For ease of visualization, all r values were normalized to the maximum r value measured in the study (r = 0.900). Circle size is proportional to an individual’s proportion flying time (PFT). Resultant group R∗(weighted r) vector (gray wedge) is only shown for group(s) with significant group directionality (p < 0.05). For ease of visualization, all R∗ vectors are normalized to the highest group R∗ value (R∗ = 1.472 for directional fall fliers tested in sunny conditions).

Figure 2

Time-of-day-dependent flight orientation reveals differential skylight cue processing throughout the annual cycle (A–C) Orientation plots for all summer, fall, and overwintering monarchs tested in sunny conditions. All individuals tested in sunny conditions are included regardless of individual directionality or flight scores. Circle color indicates the time of day at which the individual was tested (ranging from ∼900 to 1,600 h). Individuals within a group were randomly tested across several days.

Figure 3

Sustained flight and orientation-motivated flight are additional components of migratory flight behavior (A) Proportion flying time (PFT) for summer non-migrants, fall migrants, and overwintering migrants tested in sunny conditions. ∗p < 0.05. Boxplots are as in Figure 1. (B) Weighted r versus theta for fall migrants tested in sunny conditions. Grey shading represents 95% confidence interval. (C–E) Orientation plots for all individuals tested in sunny conditions. Individual butterflies are represented by circles colored by membership score based on PFT.

Figure 4

A model for modular dynamic switches that control migratory flight behavior Four distinct switches characterize differences between monarch behavioral states. Switch 1: seasonal plasticity generates spring/fall non-migratory versus fall migratory monarchs. Switch 2: differential processing of skylight cues leads to time-of-day dependent versus independent (or oriented) flight. Switch 3: Specific orientation direction, in both time-of-day dependent (sun-directed versus axial) and independent (southwest versus northeast) flight. Switch 4: sustained versus local flight behavior.