4.1 The refined structure of the compound eye is responsible for the CPLV
In order to improve the capture and absorption efficiency of CPL, the mantis shrimp compound eye has inevitably evolved the morphological features that can enhance CPL sensitivity (Honkanen et al., 2014). TheO. oratoria compound eye is divided into two almost perfectly symmetric halves by a mid-band to create triphasic vision, but the mid-band with CPL-recognition consists of only two rows of ommatidia, which is sparse compared to the many mantis shrimps (such as Gonodactyloidae) (Marshall, 1988; Chiou et al., 2008; Graydon, 2009; Templin, 2017). Thus, we speculate that the CPLV of O. oratoriamay be weakened. Previous study confirmed that the PL in water is predominately caused by the scattering of various particles (Ivanoff and Waterman, 1958, Cronin et al., 2003), and the polarization degree of light in turbidity water (usually not above 30%) was significantly lower than that in clear water (reach to 60%) (Ivanoff and Waterman, 1958, Cronin et al., 2003).O. oratoria are known to live in relatively high turbidity environments and thus may experience less CPL throughout its evolutionary process than other mantis shrimp species living in relatively clear water, which indirectly leads to the “disuse” of CPLV-related mid-band in O. oratoria .
The relatively large ommatidium area (width ~ 800 μm) appears to enhance the capture efficiency of O. oratoria compound eye to photon (McIntyre and Caveney, 1998). Although we did not perform the validation experiment for ommatidia function in O. oratoria , related study has been accurately established in the ommatidia of other mantis shrimps (Templin, 2017). Each ommatidium resembles a cylindrical structure, which also increases the possibility of photon capture. We observed that the microvilli in the rhabdom are orthogonal geometric interleaved, this array has been proved to be very valuable for the transmission and recognition process of CPL due to it can facilitates the ability to detect two or more e-vector orientations (Kleinlogel, 2006; Templin, 2017). It is worth noting that two different shapes (square and oval) of rhabdom were captured in the electron microscopic section of ommatidia, which may be derived from R1-7 and R8 retinular cells, respectively (Liu and Ding, 2015). Previous studies have demonstrated that the short oval rhabdom can act as a quarter-wave plate and convert the received CPL into LPL (Cronin et al., 1991). Hence, the O. oratoria compound eye has microstructures that can recognize CPL, and these structures can ensure that the compound eye can accurately distinguish the angle of light after detecting CPL, and convert CPL into easily recognized LPL.
4.2 The potential order of light utilization byO. oratoria compound eye
The expression levels of vision-related functional genes and proteins are light scenario-specific, so the identified DEGs and DEPs may regulate the light recognition process of O. oratoria compound eye. Based on the annotation information, visual regulation-related DEGs and DEPs mainly appear in NL-vs-DL and LCPL-vs-DL, especially in NL-vs-DL. This may mean that O. oratoria compound eye use NL and LCPL over LPL and RCPL, although LCPL needs to be converted to LPL for further recognition. This is puzzling because any areas (whether dorsal, ventral, or midband) of the mantis shrimp compound eye have been shown to recognize the LPL (Marshall, 1988; Chiou et al., 2008; Graydon, 2009; Templin, 2017). Meanwhile, orthogonal geometric interlace rhabdom were also found in the O. oratoria ommatidia, suggesting that theO. oratoria has the LPL recognition ability. There may be two explanations for this, including (1) the lack of reference genome forO. oratoria or other mantis which limited the comparative transcriptomic and proteomic analyses, and no annotations were found for functional genes or proteins that can recognize LPL. (2) LPL is an “ecological trap (Dwernychuk and Boag, 1972)” of O. oratoria , which is a very bold hypothesis without further proof. In fact, we repeated three breeding experiments and found that the mortality rate ofO. oratoria s exposed to LPL was close to 50%, while the mortality rate of O. oratoria s exposed to other light scenarios was almost 0. Therefore, we suspected that the “ecological trap” caused by LPL is more likely to be a behavioral phenomenon ofO. oratoria (Battin, 2004; Robertson and Hutto, 2006). Specifically, the attractiveness of LPL toO. oratoria may not be commensurate with its suitability for survival and reproduction (Levins, 1968, Witherington, 1997), and may even lead to the death of mantis shrimp. This “polarization captivity effect” has been demonstrated in a variety of animals and are responsible for their continued death (Kriska et al., 2006; Horváth et al., 2011; Robertson et al., 2017), but was not measured here. While further research and validation is needed, from our results we speculate that the order of light utilization by O. oratoria compound eye is NL, LCPL, LPL, RCPL and DL.
4.3Opsin is the first stage of CPL perception
We found significant changes in the expression of some opsin genes and related proteins in O. oratoria compound eyes exposed to LCPL, suggesting that opsin is critical for CPL recognition in O. oratoria compound eye. Photon acquisition and absorption by opsin initiates the visual transduction cascade mechanism (Zang and Neuhauss, 2021), the physical stimuli generated by photons are subsequent converted into biological signals and then regulate the neurotransmitter glutamate released by photoreceptor synapses (Burns and Maylor, 2001; Lamb and Pugh, 2006; Fu and Yau, 2007), which will ultimately be received by the brain. In this process, opsins belonging to the G protein–coupled 7-transmembrane receptor family are typically covalently bound to retinal-binding proteins (formed by vitamin A1 11-cis-retinal and Schiff base) to form photopigment complexes called visual pigment (Figure.7; Farrens et al., 1996; Bowmaker and Hunt, 2006; Liu et al., 2007; Peña et al., 2016).