1. Introduction
Visual organs are crucial for
survival in animals. Due to visual tasks, including predation, avoidance
of enemies, movement and reproduction, the visual organs of some animals
have evolved special features such as stereoscopic vision (Nityananda et
al., 2018), peripheral vision (Banks et al., 2015), rapid saccade
(Jonathan et al., 2019) and visual illusion (Endler et al., 2010).
Visual organs of some animals have even evolved to recognize peculiar
optical signaling, such as polarized light (PL) (Gagnon et al., 2015;
Templin, 2017). PL is another property of natural light (NL) that is
scattered during transmission, and PL can be divided into linearly
polarized light (LPL), circularly polarized light (CPL) and elliptically
polarized light according to the trajectory shape of PL vector (Wang et
al., 2013). PL was once overlooked because the human eye can not
directly identify it. However, behavioral, morphological, and
electrophysiological experiments have hypothesized that PL can help
animals with polarization-sensitive visual system enhance the contrast
between objects and the environmental background (Shashar et al., 2011,
Marshall and Cronin, 2014), thereby ”secretly” conducting directional
navigation (Homberg, 2015), camouflage (Chiao et al., 2011), target
detection (How et al., 2015), mate selection (Calabrese et al., 2014),
and other visual tasks. It is worth noting, though, that polarization
sensitivity is not the same as polarization
vision. The difference lies in
whether animals can accurately discern the angle of light after
detecting PL (Templin, 2017). That means there are fewer animals with
polarization vision, especially CPL
vision (CPLV). Although the wings of golden turtle beetles seem to have
the ability to reflect CPL (Brady and Cummings, 2010; Jiang et al.,
2012), they can’t recognize it (Miklós et al., 2012). There are more
than 400 mantis shrimp species
(Arthropoda: Crustacea) in the world,
and to the surprise of the researchers, is the only animal found to
reflect and also recognize CPL (Chiou et al., 2008; Graydon, 2009;
Thoen, 2014).
A previous behavioral study has
found that a large proportion (up to 85%) of the Philippine mantis
shrimp (Gonodactylaceus
falcatus ) show an instinctive avoidance to caves that emit CPL (Gagnon
et al., 2015). The carapace (i.e. appendage, telson) of mantis shrimp
has also been found to reflect CPL and the reflex ability is
gender-specific (Graydon, 2009; Gagnon et al., 2015). Interestingly, CPL
reflected from mantis shrimp carapace can only be recognized by members
of the same or related species, which implies that CPL is a
communication signaling unique to mantis shrimps (Gagnon et al., 2015).
In fact, mantis shrimps spend most of their life cycle in burrows, which
become their exclusive territory to effectively hide and defend
themselves against enemies (Zhao et al., 2019). Therefore, it is safe to
speculate that the CPL reflected in the burrow is a guard signal for
mantis shrimps outside the cave that the cave is occupied by a mantis
shrimp. In conclusion, it seems that CPL signaling can help mantis
shrimp expand their visual field in the dark seafloor and then
accurately find suitable caves, which effectively reduces competition
among the ferocious mantis shrimps.
The mid-band ommatidia of compound eye are the critical structure for
the mantis shrimp to recognize CPL (Marshall, 1988). Previous
morphological studies on the mantis shrimp (i.e. Odontodactylus
cultrifer , Lysiosquillina maculate ) compound eyes have shown
that the angle between the direction of the distal rhabdom of R8
retinular cell and the proximal rhabdom of (R1, 4, 5) and (R2, 3, 6, 7)
retinular cells in the mid-band ommatidia was +45° and -45°,
respectively (Marshall, 1988; Chiou et al., 2008; Graydon, 2009).
Meanwhile, the distal rhabdom of R8 retinular cell shows a special short
oval shape and can act as a quarter-wave plate (Chiou et al., 2008).
This impressive array of rhabdom array and shape can convert CPL
received by R8 retinular cell into LPL that can be easily recognized by
R1~R7 retinular cells (Graydon, 2009; Gagnon et al.,
2015). Additionally, the
duplication of opsin genes and parallel substitution of functional amino
acid sites that are positively selected for CPL may also be responsible
for the CPLV of the mantis shrimp (Yuan et al., 2010; Briscoe et al.,
2010). In the mid-band retinular cells of the Gonodactylus
smithii and Odontodactylus scyllarus compound eyes, there are 6
middle wavelength opsins (MWSs) and 15 MWS genes have been
confirmed (Porter et al., 2009; Cronin et al., 2010). Meanwhile, Porter
et al. (2009) speculated that the mantis shrimp has also undergoneMWS genes duplication during the CPL adaptation, and newMWS genes with CPL recognition function have been generated, but
these theories have not been proven.
As a representative of the mantis shrimp, Oratosquilla oratoria(De Haan, 1844) is widely distributed in the coastal waters of China and
has highly developed compound eyes. Although the mid-band of theO. oratoria compound eye only has two rows of ommatidia (Marshall
et al., 2007; Fu et al., 2019; Zhao et al., 2019), it is still an
excellent model for CPL recognition mechanism research. In this study,
we aimed to elucidate the critical CPL-recognition mechanisms of theO. oratoria and other mantis shrimp species at the morphological
and molecular levels. The microscopic structure of the O.
oratoria compound eye was observed for the first time, and
transcriptome and proteome sequencing were performed for the O.
oratoria compound eye exposed to five lighting conditions. Here we
providing key knowledge to understand the formation and evolution of
CPLV and CPLV-manipulation visual tasks in mantis shrimps.