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 20! 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 25! 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 30! 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 35! 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 40! 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. 45!

How to Become a Crab: Phenotypic Constraints on a Recurring Body Plan

“…As of yet, molecular phylogenetics has been insufficient to resolve the puzzle of podotremes, therefore our depiction of their extant relationships in Figure 2 relies on morphological data. Anatomically, these crabs lie in between Anomura and Eubrachyura, though all current data strongly support a paraphyletic podotreme grade with brachyuran affinity (Luque et al 2019a). Analysis of eight Sanger sequenced genes including 58 of ~100 brachyuran families (Tsang et al 2014), analyses of mitogenomes (Tan et al 2018b(Tan et al , 2019, and a recent transcriptomic analysis (Ma et al 2019) each recovered podotreme paraphyly (the former with weak support).…”

“…Of 11 extant podotreme families, however, over one third lack molecular data: no sequences have been published for Poupiniidae, Lyreididae, and Phyllotymolinidae, and only a single 18S sequence is available for Homolodromiidae. Meanwhile, morphological trees, including fossils, have sampled more extensively from podotreme lineages (Luque et al 2019a(Luque et al , 2019b). Thus, a major goal of future research should represent all meiuran families with morphological data, and all extant families with strongly supported phylogenomic data, for a well-resolved total evidence phylogeny.…”

How to become a crab: Phenotypic constraints on a recurring body plan

“…Anatomically, these crabs lie in between Anomura and Eubrachyura, and all current data strongly support a paraphyletic podotreme grade with brachyuran affinity. [31] Analysis of eight Sanger sequenced genes including 58 of ∼100 brachyuran families, [27] analyses of mitogenomes, [30,32] and a recent transcriptomic analysis [33] each recovered podotreme paraphyly (the former with weak support). Relationships recovered among podotremes were entirely contradictory between those analyses.…”

“…Meanwhile, morphological trees, including fossils, have sampled more extensively from podotreme lineages. [2,31] Thus, a major goal of future research should represent all meiuran families with morphological data, and all extant families with strongly supported phylogenomic data, for a well-resolved total evidence phylogeny.…”

New hypotheses concerning the earliest brachyurans (Crustacea, Decapoda, Brachyura)

“…Van Bakel et al (2012b: 156, figs 57A-D, 58A-D, 59A, B, 61A) were the pioneers in illustrating the spermathecae in the Palaeocorystoidea. While spermatheca are known in Dakoticancroidea (Guinot 1993a;Guinot & Tavares 2001;Artal et al 2008;Schweitzer et al 2019), in Etyidae (Guinot & Tavares 2001), and in Diaulacidae Wright & Collins, 1972(in Diaulax carteriana Bell, 1863 from the Coniacian-Campanian, see Karasawa et al 2011: fig. 5A), we have no idea about the spermathecae in fossil Dynomenidae Ortmann, 1892 and Homolodromiidae, in Prosopidae, Tanidromitidae, and in Goniodromitinae, as well as in all families of Glaessneropsoidea Patrulius, 1959. Is it true that "All Jurassic and almost all Cretaceous crabs belong to Dromiacea", as stated by Krobicki & Zatoń (2016: 695), in accordance with now widely accepted perceptions?…”