159
Quantum Compass of Migratory Birds
a singlet radical pair (•D+ and •A–)S is formed. Te absorption of blue light promotes electron transfer
to an acceptor molecule (A), resulting in a singlet radical pair. An external magnetic feld afects the S-T
conversion. Te inset gives a possible dependency of the triplet yield from the angle of the radical pair to
the external magnetic feld. Tus, the S-T conversion leads to a triplet radical pair (•D+ and •A–)T, with
the triplet yield depending on the alignment of the molecules in the external magnetic feld. Here triplet
products are chemically diferent from the singlet products and thus may play a role in magnetorecep
tion. Tat is, when a photoreceptor, favin (•D+) is excited by blue light, radical pair is generated when
electron transfer occurs from nearby Trp (•A–). Te S-T conversion is afected by the external mag
netic felds (Zeeman interaction), and the hyperfne coupling (HPC). Tis S-T conversion is magnetic
feld strength-dependent (Brocklehurst, 1976; Werner et al., 1978, 1983; Lewis et al., 2018; Hore, 2019).
Teoretically, it has been clarifed that the efciency of the mixing process of a singlet-born radical pair
into a triplet spin state is maximized in a relatively weak magnetic feld (Timmel et al., 1998; Timmel and
Henbest, 2004; Evans et al., 2013; Lewis et al., 2018; Kerpal et al., 2019).
In chemical terms, the minimum requirement for a radical pair reaction to be sensitive to an exter
nal magnetic feld is that at least one of the S and T states undergoes a reaction that is not open to the
other, usually as a consequence of the imperative to conserve spin angular momentum (Rodgers and
Hore, 2009). A simple reaction scheme that could form the basis of a compass magnetoreceptor is
shown by Rodgers and Hore (2009). Here, (A) and (B) could be portions of the same molecule or dis
tinct molecules held in close proximity by their surroundings (e.g., two cofactors or a cofactor and an
amino acid residue in a protein) (Rodgers and Hore, 2009). (C) is either the signaling state or leads to
the signaling state via subsequent chemical transformations (which are not shown) (Rodgers and Hore,
2009). An applied magnetic feld can alter the yield of (C) by regulating the competition between its
formation (from the S and T states, step 4), and the regeneration of (A) (B) (exclusively from the S state,
step 2) (Rodgers and Hore, 2009). If the S-T interconversion is hindered by the external magnetic feld,
then less (C) will be produced and correspondingly more radical pairs recombine directly to (A) (B)
(Rodgers and Hore, 2009). Te opposite follows if the feld enhances the S-T interconversion (Rodgers
and Hore, 2009). It is important to note that the external magnetic feld is far too weak to initiate new
radical reactions (Rodgers and Hore, 2009). Variants on the reaction scheme are possible, and although
the details of the chemistry may difer, the principles remain the same (Rodgers and Hore, 2009).
Some of the more likely alternatives include an excited triplet precursor state; electron transfer in the
reverse direction to form A•−B•+; and formation of the radical pair via sequential electron transfer steps
(Solov’yov et al., 2007).
Spin dynamics simulations of anisotropic reaction yields for the RPM model are shown by Rodgers
and Hore (2009), compiled from Rodgers (2007) and Efmova and Hore (2008). Here, upper images
indicate polar plots; lower images show the corresponding signal modulation patterns for a bird looking
directly along the GMF vector. Te heights of the vertical scale bars in the upper images correspond to
singlet yields of 2% or 0.2%. Te simulations demonstrate that a relatively simple orientation depen
dence of the reaction yield (A) can be obtained from radical pairs containing a small number of hyper
fne interactions or from more complex radicals when a few symmetry-related hyperfne interactions
dominate (B). More intricate anisotropy patterns (C) can be dramatically simplifed if the radical pairs
are axially rotationally disordered (D). Te signal modulation pattern for C is identical to that for D
and is only shown once. Note that in all cases the reaction yield is invariant to the exact reversal of the
magnetic feld vector, i.e., the response is that of an inclination compass rather than a polarity compass.
Unless the radicals contain very few magnetic nuclei or possess some degree of molecular symmetry or
are favorably disordered, the shape of the anisotropy can be complex (Rodgers and Hore, 2009). Tere
is no clear picture of what would constitute the optimum sensory input for the bird; however, it seems
reasonable to suppose that strongly anisotropic but relatively simple directional information would be
favored (Rodgers and Hore, 2009). Simulations and experiments on solution-phase reactions suggest a
few simple design features discussed in the section on CRYs (Cintolesi et al., 2003; Efmova and Hore,
2008; Rodgers et al., 2007).