Connecting the Navigational Clock to Sun Compass Input in Monarch Butterfly Brain

Abstract

Migratory monarch butterflies (Danaus plexippus) use a time-compensated sun compass to navigate to their overwintering grounds in Mexico. Although polarized light is one of the celestial cues used for orientation, the spectral content (color) of that light has not been fully explored. We cloned the cDNAs of three visual pigment-encoding opsins (ultraviolet [UV], blue, and long wavelength) and found that all three are expressed uniformly in main retina. The photoreceptors of the polarization-specialized dorsal rim area, on the other hand, are monochromatic for the UV opsin. Behavioral studies support the importance of polarized UV light for flight orientation. Next, we used clock protein expression patterns to identify the location of a circadian clock in the dorsolateral protocerebrum of butterfly brain. To provide a link between the clock and the sun compass, we identified a CRYPTOCHROME-staining neural pathway that likely connects the circadian clock to polarized light input entering brain.

Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes

“…In Drosophila (Wernet et al, 2003) and monarch butterflies (Sauman et al, 2005), the ommatidia of the DRA have a unique pattern of opsin expression compared to the main retina -this region contains ommatidia with rhabdoms specialized for polarization vision (Labhart and Meyer, 1999;Stalleicken et al, 2006). One possible explanation for the dramatically altered pattern of opsin mRNA expression we identified in the dorsal part of the L. rubidus eye is that it represents an expansion of the DRA.…”

“…Unlike the unusual BRh1 mRNA expression in the outer R3-8 photoreceptor cells of the L. rubidus dorsal eye, the typical lepidopteran expresses short wavelength opsin mRNAs only in the R1 and R2 cells (Kitamoto et al, 2000;Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005). Closer inspection of UVRh, BRh1 and BRh2 expression in individual ommatidia indicated that these transcripts are also present in the R1 and R2 photoreceptor cells of both sexes (Fig.·4).…”

“…We note that the short wavelength opsins have a lysine at residue 112 (UVRh) and a glutamate at residue 107 (BRh1 and BRh2), which confer UVabsorbing (lysine) and blue-absorbing (glutamate) spectra (Salcedo et al, 2003). The situation in L. rubidus differs markedly from that of the nymphalid butterflies Vanessa cardui or the monarch Danaus plexippus, in which only three opsin mRNAs are expressed (UV, B, and LW) in the photoreceptor cells of the adult eye (Briscoe et al, 2003;Sauman et al, 2005), or that of the swallowtail butterfly, in which three duplicate LW opsin genes are expressed (Briscoe, 1998;Kitamoto et al, 1998). The L. rubidus opsin expression pattern does, however, resemble the situation in Pieris rapae, in which duplicate B opsin genes are also expressed in the eye (Arikawa et al, 2005) (but see below).…”

“…To explain the four major evolutionary innovations we have identified in L. rubidus eye (duplicate blue opsin cDNAs, novel R1 and R2 photoreceptor subtypes, co-expression of B and LW opsins and male-only BRh1 opsin expression in R3-8 cells) we M. P. Sison-Mangus and others propose the following evolutionary scheme (Fig.·6): Nymphalids, the closest outgroup for which gene expression data are available, have three kinds of ommatidia: UV and B opsin mRNAs are expressed in R1 and R2 photoreceptor cells in a non-overlapping fashion, and the LW opsin mRNA is expressed in the R3-8 photoreceptor cells (Briscoe et al, 2003;Sauman et al, 2005;Zaccardi et al, 2006). This pattern is also found in the moth Manduca sexta , and likely represents the ancestral lepidopteran eye plan.…”

“…Most lepidopteran eyes contain a minimum of three visual pigments with absorbances that peak at ~350·nm (UV), 440·nm (blue, B) and 530·nm (long wavelength, LW) (reviewed in Briscoe and Chittka, 2001). In the sphingid moth, the painted lady and monarch butterfly, these visual pigments are encoded by paralogous UV, B and LW opsin genes, which were present in the ancestor of all lepidopterans (Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005). Deviations from this basic plan have been described in the most primitive of butterfly families, the papilionids, in which two rounds of duplication of the LW eye opsin gene have occurred (Briscoe, 1998;Kitamoto et al, 1998;Briscoe, 2001); and in the pierids, in which a duplicate blue opsin gene has been reported (Arikawa et al, 2005).…”