Molecular diversity of visual pigments in Stomatopoda (Crustacea)

Journal of Experimental Biology

Zhang

Desai

et al. 2010

Self Cite

SUMMARYStomatopod crustaceans have complex and diverse visual systems. Among their many unique features are a specialized ommatidial region (the midband) that enables the eye to have multiple overlapping visual fields, as well as sets of spectral filters that are intercalated at two levels between tiers of photoreceptors involved in polychromatic color vision. Although the physiology and visual function of stomatopod eyes have been studied for many years, how these unique visual features originated and diversified is still an open question. In order to investigate how stomatopods have attained the current complexity in visual function, we have combined physiological and morphological information (e.g. number of midband rows, number of filters in the retina, and the spectral properties of filters) with new phylogenetic analyses of relationships among species based on nucleotide sequence data from two nuclear (18S and 28S rDNA) and two mitochondrial [16S and cytochrome oxidase I (COI)] genes. Based on our recovered phylogenetic relationships among species, we propose two new superfamilies within the Stomatopoda: Hemisquilloidea and Pseudosquillodea. Maximum likelihood ancestral state reconstructions indicate that ancestral stomatopod eyes contained six midband rows and four intrarhabdomal filters, illustrating that the visual physiological complexity originated early in stomatopod evolutionary history. While the two distal filters contain conservative sets of filter pigments, the proximal filters show more spectral diversity in filter types, particularly in midband row 2, and are involved in tuning the color vision system to the photic environment. In particular, a set of related gonodactyloid families (Gonodactylidae, Protosquillidae, Takuidae) inhabiting shallow, brightly lit coral reef waters contain the largest diversity of filter pigments, which are spectrally placed relative to the underlying photoreceptors to take advantage of the broad spectrum of light available in the environment.

Section: Introductionmentioning

confidence: 99%

Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans

Journal of Experimental Biology

Zhang

Desai

et al. 2010

Self Cite

“…Evolutionary history of stomatopod crustacean opsins, illustrating a separation between opsins involved in colour vision from those expressed in photoreceptors specialized for the detection of polarized light (for more detail, see [57]). Phylogeny is derived from Porter et al [58]. Stomatopod opsins form six groups, labelled A-F, and the sequence groups (triangles) have been shaded grey.…”

Section: Photoreceptors As Polarization Detectors: the Composition Anmentioning

confidence: 99%

“…Preliminary studies indicate that the genes expressed in polarization-sensitive photoreceptors are evolutionarily distinct from those in colour-sensitive photoreceptors (figure 4). Furthermore, comparative evolutionary analyses have identified a set of amino acids that are diversifying among stomatopod opsins that are likely to interact with machinery inside the cell, either in the phototransduction system or with cytoskeletal elements similar to the Drosophila signalplex [58].…”

Section: Photoreceptors As Polarization Detectors: Visual Pigment Dimmentioning

confidence: 99%

The molecular basis of mechanisms underlying polarization vision

Roberts

Cronin

2011

Phil. Trans. R. Soc. B

Self Cite

The underlying mechanisms of polarization sensitivity (PS) have long remained elusive. For rhabdomeric photoreceptors, questions remain over the high levels of PS measured experimentally. In ciliary photoreceptors, and specifically cones, little direct evidence supports any type of mechanism. In order to promote a greater interest in these fundamental aspects of polarization vision, we examined a varied collection of studies linking membrane biochemistry, protein -protein interactions, molecular ordering and membrane phase behaviour. While initially these studies may seem unrelated to polarization vision, a common narrative emerges. A surprising amount of evidence exists demonstrating the importance of protein -protein interactions in both rhabdomeric and ciliary photoreceptors, indicating the possible long-range ordering of the opsin protein for increased PS. Moreover, we extend this direction by considering how such protein paracrystalline organization arises in all cell types from controlled membrane phase behaviour and propose a universal pathway for PS to occur in both rhabdomeric and cone photoreceptors.

“…Electrophysiological studies have detailed the spatial variation of polarization sensitivity in the different photoreceptor classes in the eye (Kleinlogel and Marshall, 2006;Chiou et al, 2008). Optical measurements Chiou et al, 2008), optical modeling ) and molecular methods (Porter et al, 2009;Roberts et al, 2011) have provided additional information on the underlying mechanisms of polarization sensitivity. Optical techniques have also shown that many species of stomatopod produce visual signals that are either linearly or circularly polarized (Chiou et al, 2005;Chiou et al, 2008;Cronin et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Out of the blue: the evolution of horizontally polarized signals inHaptosquilla(Crustacea, Stomatopoda, Protosquillidae)

How

Journal of Experimental Biology

Radford

et al. 2014

Self Cite

The polarization of light provides information that is used by many animals for a number of different visually guided behaviours. Several marine species, such as stomatopod crustaceans and cephalopod molluscs, communicate using visual signals that contain polarized information, content that is often part of a more complex multidimensional visual signal. In this work, we investigate the evolution of polarized signals in species of Haptosquilla, a widespread genus of stomatopod, as well as related protosquillids. We present evidence for a pre-existing bias towards horizontally polarized signal content and demonstrate that the properties of the polarization vision system in these animals increase the signal-to-noise ratio of the signal. Combining these results with the increase in efficacy that polarization provides over intensity and hue in a shallow marine environment, we propose a joint framework for the evolution of the polarized form of these complex signals based on both efficacy-driven (proximate) and content-driven (ultimate) selection pressures. KEY WORDS: Stomatopod, Mantis shrimp, Polarization vision, Signal evolution, Sensory bias, Multi-modal signal INTRODUCTIONPolarization sensitivity is a common visual specialization that has evolved in both terrestrial and aquatic animals, and is particularly prevalent in invertebrates (Wehner and Labhart, 2006). On land, many insects use the celestial polarization pattern for navigation (Wehner, 1976;Rossel and Wehner, 1986;Labhart and Meyer, 1999;Dacke et al., 2003), while in the ocean, some crustaceans and cephalopod molluscs use polarization information to detect prey and possibly as a means of conspecific communication (Shashar et al., 1996;Cronin et al., 2003a;Chiou et al., 2007;Mäthger et al., 2009;Cronin et al., 2009;Chiou et al., 2011). In the context of communication, polarization often forms composite signals with other visual dimensions, such as hue and brightness (Cronin et al., 2003a;Cronin et al., 2009).The term polarization is used to define several properties of light. The angle of polarization describes the predominant direction in which the electric field of the light oscillates, while the degree of polarization defines the extent to which waves oscillate at the same angle. Underwater, differential sensitivity to either angle or degree of polarization has several fundamental advantages over other forms of visual information (Cronin et al., 2003a;Cronin et al., 2003b;Cronin et al., 2009;Shashar et al., 2011). For instance, in shallow, clear marine waters, the intensity and spectral composition of the downwelling light can vary dramatically, both as a function of the time of day, and because of environmental factors such as turbidity (Cronin et al., 2014). In such changing conditions, the polarization of light remains more constant than other visual dimensions over short ranges (Waterman, 1954;Cronin, 2001), which renders it a reliable provider of information (Shashar et al., 2011;Johnsen et al., 2011). Previous research in this field has fo...