Evolution of crab eye structures and the utility of ommatidia morphology in resolving phylogeny

ABSTRACT Image-forming compound eyes are such a valuable adaptation that similar visual systems have evolved independently across crustaceans. But if different compound eye types have evolved independently multiple times, how useful are eye structures and ommatidia morphology for resolving phylogenetic relationships? Crabs are ideal study organisms to explore these questions because they have a good fossil record extending back into the Jurassic, they possess a great variety of optical designs, and details of eye form can be compared between extant and fossil groups. True crabs, or Brachyura, have been traditionally divided into two groups based on the position of the sexual openings in males and females: the so-called ‘Podotremata’ (females bearing their sexual openings on the legs), and the Eubrachyura, or ‘higher’ true crabs (females bearing their sexual openings on the thorax). Although Eubrachyura appears to be monophyletic, the monophyly of podotreme crabs remains controversial and therefore requires exploration of new character systems. The earliest podotremous lineages share the plesiomorphic condition of ‘mirror’ reflecting superposition eyes with most shrimp, lobsters, and anomurans (false crabs and allies). The optical mechanisms of fossil and extant podotreme groups more closely related to Eubrachyura, however, are still poorly investigated. To better judge the phylogenetic utility of compound eye form, we investigated the distribution of eye types in fossil and extant podotreme crabs. Our findings suggest the plesiomorphic ‘mirror’ eyes—seen in most decapod crustaceans including the earliest true crabs—has been lost in several ‘higher’ podotremes and in eubrachyurans. We conclude that the secondary retention of larval apposition eyes has existed in eubrachyurans and some podotremes since at least the Early Cretaceous, and that the distribution of eye types among true crabs supports a paraphyletic podotreme grade, as suggested by recent molecular and morphological phylogenetic studies. We also review photoreceptor structure and visual pigment evolution, currently known in crabs exclusively from eubrachyuran representatives. These topics are critical for future expansion of research on podotremes to deeply investigate the homology of eye types across crabs.