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Review
. 2012 Apr;22(2):353-61.
doi: 10.1016/j.conb.2011.11.009. Epub 2011 Dec 9.

Unraveling navigational strategies in migratory insects

Affiliations
Review

Unraveling navigational strategies in migratory insects

Christine Merlin et al. Curr Opin Neurobiol. 2012 Apr.

Abstract

Long-distance migration is a strategy some animals use to survive a seasonally changing environment. To reach favorable grounds, migratory animals have evolved sophisticated navigational mechanisms that rely on a map and compasses. In migratory insects, the existence of a map sense (sense of position) remains poorly understood, but recent work has provided new insights into the mechanisms some compasses use for maintaining a constant bearing during long-distance navigation. The best-studied directional strategy relies on a time-compensated sun compass, used by diurnal insects, for which neural circuits have begun to be delineated. Yet, a growing body of evidence suggests that migratory insects may also rely on other compasses that use night sky cues or the Earth's magnetic field. Those mechanisms are ripe for exploration.

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Figures

Figure 1
Figure 1. Sensory cues used for long-distance orientation by migratory insects
(a) Several insect species undergo seasonal long-distance migration, including (from left to right) the monarch butterfly, other day-active butterflies, nocturnal moths, the desert locust, and dragonflies. Monarch picture: courtesy of Monarch Watch (www.monarchwatch.org). (b) Migratory insects exploit environmental cues for long-range navigation. (Top left) Migrants flying during the day can extract directional information from the sun position in the sky (yellow oval), as well as the derived patterns of polarized skylight (E-vector; dashed lines) and the spectral gradient, which ranges from longer wavelengths of light (green) dominating in the solar hemisphere to shorter wavelengths (violet) dominating in the antisolar hemisphere. The bar thickness of dashed lines represents the degree of polarization, while the bar orientation represents the angle of polarization relative to solar position as viewed from the center of the celestial sphere. Modified from [20••]. (Bottom left) The moon and its polarization pattern, stars and the Milky Way are celestial cues available to migratory insects flying at night. (Right) The Earth's magnetic field emerges from the southern hemisphere, wraps around the globe and re-enters at the northern hemisphere (blue lines). Migrating animals can extract directional information (compass sense) and positional information (map sense) from the polarity, inclination and intensity of the Earth's magnetic field, which are gradually changing across the Earth's surface (represented by the angle and length of the violet arrows). Modified from [41].
Figure 2
Figure 2. Neuronal organization of the insect sun compass
(a) Simplified schematic of the polarization vision pathway in a frontal view of the desert locust brain. Highlighted in yellow are brain regions involved in processing of compass information. Key neural projections of the polarization vision pathway are shown as solid lines. Filled circles indicate proposed output and open semicircles indicate proposed input sites. Blue: input stage neurons; green: intermediate stage neurons; red: output stage neurons. Note that for clarity inputs are represented in the left hemisphere, while outputs are shown in the right hemisphere. The inset illustrates the mapping of zenithal E-vectors in the columns of the protocerebral bridge (PB). CBU, upper division of the central body; CBL, lower division of the central body; MB, mushroom body; La, lamina; Me, medulla; aMe, accessory medulla; Lo, lobula; LoX, lobula complex; AOTu, anterior optic tubercle; LAL, lateral accessory lobe; LT, lateral triangle; pPC, posterior protocerebrum; AL, antennal lobe. (b) E-vector tuning (black bidirectional arrow) and azimuth tuning (colored arrows) of an input stage compass neuron from the locust (green stimulation and ultraviolet stimulation). E-vector tuning was determined by presenting a rotating polarizer from the zenith (blue light), and azimuth tuning was determined by presenting an unpolarized light-spot that moved around the animal at constant elevation. The tuning angle was defined as the maximal activity during stimulus presentation (mean angle of Rayleigh-test). The angle between E-vector tuning and azimuth tuning (response to green light spot) is defined as |ΔΦmax|-value. (c) Time dependent adjustment of E-vector tunings in neurons of the input stage of the compass network of the locust. Plotted is the |ΔΦmax|-value against the recording time of neuron. The red line represents a celestial ΔΦ function fitted to the data, describing the angular difference between solar azimuth and E-vector orientation for individual points of an ideal natural sky, calculated for the season from which the locusts had been reared. The fit line was calculated for 60° elevation above the horizon according to the visual axis of the locust DRA and for the Tropic of Cancer (23.4°N), its natural habitat. Number of recordings is indicated in bars (mean ± SD). Modified from [27]. (d) Polarization vision pathway in the monarch butterfly brain. Colors and symbols as in (a). (e and f) E-vector tuning and azimuth tuning (e), and adjustment of E-vector tuning over the course of the day (f) for the monarch butterfly. Symbols as in (b and c). The angle between E-vector tuning and mean azimuth tuning is defined as |ΔΦmax|-value. Polarized light was presented in the ultraviolet range. The red line in (f) represents the prediction of the angular difference between the mean perceived E-vector for the region of sky viewed by the monarch DRA and the solar azimuth over the course of the day. The values were calculated for the latitude and season from which migratory monarchs had been captured. ZT, Zeitgeber time of the 11-hr light:13-hr dark lighting cycle in which the monarchs have been maintained; 0 represents lights on. Bars, mean ± SD. Modified from [20••].
Figure 3
Figure 3. Integrated model of the components of the time-compensated sun compass in the monarch butterfly
Skylight input to the eye: the dorsal rim area (DRA) of the eye senses the angle of ultraviolet polarized light (crosshatched violet circle) and the main retina senses color (violet, blue and green circles) or the sun itself (without discrimination of colors). Both skylight cues are integrated and transmitted to the central complex (CX; in grey), through neural pathways that are not yet completely defined (dashed colored lines and black solid lines). Clock entrainment: Blue light entrains (synchronizes) circadian clocks in the antennae and the brain to the 24-hr day. The antennal clocks, involved in solar azimuth compensation, provide the major timing information to sun compass orientation behavior. The neural pathway connecting the antennal clocks to the CX is not yet determined (dashed red line with question mark). A minor influence of the brain clock on output neurons of the CX could be mediated through a neural pathway connecting the clock cells in the pars lateralis (PL) to the CX (blue dashed lines). In addition, the timing component of the solar elevation compensation may originate from the brain clocks in the PL (blue spots), as a CRYPTOCHROME1 positive fiber pathway (orange lines) connects the PL to the accessory medulla (aMe) and terminates in the proximity of proposed projections from the DRA [15]. The integrated signal in the central complex or its output structures is finally transmitted via descending neurons (DN) to motor circuits that generate oriented flight behavior via yet unknown pathways. Modified from [6].

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