The Monarch Butterfly as a Model for Understanding the Role of Environmental Sensory Cues in Long-Distance Migratory Phenomena

Abstract

The awe-inspiring annual migration of monarch butterflies (Danaus plexippus) is an iconic example of long-distance migratory phenomena in which environmental sensory cues help drive successful migration. In this mini-review article, I begin by describing how studies on monarch migration can provide us with generalizable information on how sensory cues can mediate key aspects of animal movement. I describe how environmental sensory cues can trigger the development and progression of the monarch migration, as well as inform sensory-based movement mechanisms in order to travel to and reach their goal destination, despite monarchs being on their maiden voyage. I also describe how sensory cues can trigger season-appropriate changes in migratory direction during the annual cycle. I conclude this mini-review article by discussing how contemporary environmental challenges threaten the persistence of the monarch migration. Environmental challenges such as climate change and shifting land use can significantly alter the sensory environments that monarchs migrate through, as well as degrade or eliminate the sources of sensory cues that are necessary for successful migration.

Spectres of Clock Evolution: Past, Present, and Yet to Come

“…The fact that cyanobacteria can transmit circadian phase to their daughter cells unimpeded through multiple cell division cycles likely facilitates this anticipation of key environmental transitions such as sunsets and sunrises (Mihalcescu et al, 2004). Of note, the phenomenon of a species being able to time itself progressively through cycles that last longer than their generational time is not exclusively prokaryotic, and has been well-studied in eukaryotes: monarch butterfly migration relies on seasonal photoperiodic cues and spans up to five generations to complete the migratory cycle (Reppert and de Roode, 2018;Guerra, 2020); similarly, diapause in many insects has been shown to be a transgenerational response (Denlinger, 1998). Cyanobacteria are, therefore, not unique in their ability to express "transgenerational rhythmicity, " although it is likely that the post-translational nature of their core clockwork -which allows for it to keep ticking unimpeded through cell division -makes them a good candidate for transgenerational transmission of temporal information.…”

Towards the Idea of Molecular Brains

“…While “this is a butterfly!” is the most common response on cards 1 and 5 of the Rorschach projective test, whose ink stains can reveal the deep structure of the human mind [ 4 , 5 , 6 ], monarch butterflies are also a gateway to quantum mechanics in biology. Thanks to their cryptochromes, which contain pairs of radicals, monarch butterflies perceive the Earth’s magnetic field and their wingbeats, can guide them over thousands of kilometres and bring us into the fascinating world of quantum biology [ 7 , 8 , 9 ]. The flapping of their wings that has also become a famous metaphor for chaos [ 10 ] could equally well illustrate the processes of cell signalling amplification, in which the weak stimulation of a receptor by a ligand or a photon, the flap of a butterfly’s wings in Brazil , can set off a cascade of molecular events that induce the overall change in the behaviour of an organism, a tornado in Texas .…”

Assaying lepidopteran flight directionality with non‐invasive methods that permit repeated use and release after testing

“…Understanding behaviour is critical for conserving species of special concern and for managing migratory or dispersive pests (Berger-Tal et al, 2011;Cooke et al, 2020). To best manage migratory species (Lennox et al, 2016), we need to understand what factors facilitate migration throughout the species range, especially species migrating long distances and through diverse landscapes (Guerra, 2020). Natural and controlled behavioural studies examining the navigational strategies of flying lepidopteran migrants (e.g., Mouritsen & Frost, 2002;Guerra et al, 2014) have enhanced our understanding of how information from environmental cues promotes successful migration.…”

“…Using fall migratory monarchs, we demonstrate how open‐loop (outdoor FS trials) and closed‐loop (DB field observations) assays, and tag‐release methods can be integrated in a repeated measures design (catch–test–release; CTR) to obtain different and complementary metrics of flight orientation from the same individual. We use monarchs to test CTR because of their well‐established southerly migratory flight directionality, which they maintain via various sensory‐based orientation mechanisms (Guerra, 2020).…”

“…We address limitations of previous work and introduce a new workflow that can increase the throughput and diversity of data acquirable from single test subjects. We describe a new, non-invasive tethering method for animals tested in FS trials (Figure 1b (Guerra, 2020).…”