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).