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.