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

Stomatopod 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.