Behavioral evidence for geomagnetic imprinting and transgenerational inheritance in fruit flies

Abstract

Certain long-distance migratory animals, such as salmon and sea turtles, are thought to imprint on the magnetic field of their natal area and to use this information to help them return as adults. Despite a growing body of indirect support for such imprinting, direct experimental evidence thereof remains elusive. Here, using the fruit fly as a magnetoreceptive model organism, we demonstrate that exposure to a specific geographic magnetic field during a critical period of early development affected responses to a matching magnetic field gradient later in life. Specifically, hungry flies that had imprinted on a specific magnetic field from 1 of 3 widely separated geographic locations responded to the imprinted field, but not other magnetic fields, by moving downward, a geotactic behavior associated with foraging. This same behavior occurred spontaneously in the progeny of the next generation: female progeny moved downward in response to the field on which their parents had imprinted, whereas male progeny did so only in the presence of these females. These results represent experimental evidence that organisms can learn and remember a magnetic field to which they were exposed during a critical period of development. Although the function of the behavior is not known, one possibility is that imprinting on the magnetic field of a natal area assists flies and their offspring in recognizing locations likely to be favorable for foraging and reproduction.

Effects of an electric field on sleep quality and life span mediated by ultraviolet (UV)-A/blue light photoreceptor CRYPTOCHROME in Drosophila

“…Nerve-specific cry expression in Drosophila increased magnetic field sensitivity 14 . A specific geographic magnetic field is imprinted on Drosophila and is inherited to its progeny 15 . The cryptochrome (cry ) gene plays a critical role in magnetic detection among diverse species.…”

Magnetic maps in animal navigation

“…In its simplest form, the hypothesis proposes that young animals imprint on the magnetic field of their natal area (Box 3), then use this information to navigate back to the region using a magnetic map as adults (Lohmann et al 2008c(Lohmann et al , 2013. In the past decade, strong evidence consistent with this idea has rapidly accumulated in several animals including salmon (Putman et al 2013(Putman et al , 2014a, sea turtles Lohmann 2015, 2018), seabirds (Wynn et al 2020), sharks (Keller et al 2021), and insects (Oh et al 2020). Indeed, the emerging picture suggests that a magnetic map sense, combined with imprinting-like learning of the magnetic field of a home region, represents a widespread solution for long-distance natal homing among migratory animals (Lohmann and Lohmann 2019).…”

“…Surprisingly, evidence consistent with magnetic imprinting has also been acquired in the fruit fly Drosophila (Oh et al 2020). Fruit flies are not known to migrate long distances, but flies do sometimes travel at least 10-15 km (Jones et al 1981;Coyne et al 1982).…”

“…Early in development, flies were exposed to one of three magnetic fields matching those that exist in different, widely separated geographic areas. Later, as adults, hungry flies responded to the field that they had experienced previously, but not to other fields, by moving downward, a geotactic behavior associated with foraging (Oh et al 2020 ). These results provide experimental evidence that organisms can learn and remember a magnetic field to which they were exposed during a critical period of development.…”

A role of cryptochrome for magnetic field-dependent improvement of sleep quality, lifespan and motor function in Drosophila

“…Nerve-specific cry expression in fruit fly, Drosophila melanogaster increased magnetic field sensitivity 9 . A specific geographic magnetic field is imprinted on Drosophila and is inherited to its progeny 10 . The cry gene plays a critical role in magnetic detection among diverse species.…”