Phylogenetic and transcriptomic analyses reveal the evolution of bioluminescence and light detection in marine deep-sea shrimps of the family Oplophoridae (Crustacea: Decapoda)
“…Despite considerable progress towards resolving the problematic phylogeny of Hippolytidae sensu lato 30 , further studies found additional polyphyly 33 , consistent in generic scope with the present analysis. The division of the older concept of Oplophoridae into two families 34 has remained controversial 35 , with one genus— Systellaspis —occupying an intermediate position between two families, as in the present analysis.Fig. 1Phylogenetic tree of Caridea.…”
Understanding the processes that shaped the strikingly irregular distribution of species richness across the Tree of Life is a major research agenda. Changes in ecology may go some way to explain the often strongly asymmetrical fates of sister clades, and we test this in the caridean shrimps. First appearing in the Lower Jurassic, there are now ~3500 species worldwide. Carideans experienced several independent transitions to freshwater from marine habitats, while many of the marine species have also evolved a symbiotic lifestyle. Here we use diversification rate analyses to test whether these ecological traits promote or inhibit diversity within a phylogenetic framework. We demonstrate that speciation rates are more than twice as high in freshwater clades, whilst symbiotic ecologies are associated with lower speciation rates. These lower rates amongst symbiotic species are of concern given that symbioses often occur in some of the most diverse, delicately balanced and threatened marine ecosystems.
“…Despite considerable progress towards resolving the problematic phylogeny of Hippolytidae sensu lato 30 , further studies found additional polyphyly 33 , consistent in generic scope with the present analysis. The division of the older concept of Oplophoridae into two families 34 has remained controversial 35 , with one genus— Systellaspis —occupying an intermediate position between two families, as in the present analysis.Fig. 1Phylogenetic tree of Caridea.…”
Understanding the processes that shaped the strikingly irregular distribution of species richness across the Tree of Life is a major research agenda. Changes in ecology may go some way to explain the often strongly asymmetrical fates of sister clades, and we test this in the caridean shrimps. First appearing in the Lower Jurassic, there are now ~3500 species worldwide. Carideans experienced several independent transitions to freshwater from marine habitats, while many of the marine species have also evolved a symbiotic lifestyle. Here we use diversification rate analyses to test whether these ecological traits promote or inhibit diversity within a phylogenetic framework. We demonstrate that speciation rates are more than twice as high in freshwater clades, whilst symbiotic ecologies are associated with lower speciation rates. These lower rates amongst symbiotic species are of concern given that symbioses often occur in some of the most diverse, delicately balanced and threatened marine ecosystems.
“…Our well-resolved dated phylogeny may inform comparative evolutionary topics, such as the evolution of visual systems in deep sea and cave environments [51,78], evolution of major body plan features [13,56,79], the role of symbiosis [80,81], evolution of behaviour [82], macroevolutionary trends through time [76,83], conservation biology and vulnerability to climate change [41,84] and more. Our new enrichment kit permits an inexpensive expansion of taxon sampling across Decapoda, via our large-scale matrix of loci conserved across 450 Myr, to accelerate discoveries in a fascinating invertebrate clade.…”
Comprising over 15 000 living species, decapods (crabs, shrimp and lobsters) are the most instantly recognizable crustaceans, representing a considerable global food source. Although decapod systematics have received much study, limitations of morphological and Sanger sequence data have yet to produce a consensus for higher-level relationships. Here, we introduce a new anchored hybrid enrichment kit for decapod phylogenetics designed from genomic and transcriptomic sequences that we used to capture new high-throughput sequence data from 94 species, including 58 of 179 extant decapod families, and 11 of 12 major lineages. The enrichment kit yields 410 loci (greater than 86 000 bp) conserved across all lineages of Decapoda, more clade-specific molecular data than any prior study. Phylogenomic analyses recover a robust decapod tree of life strongly supporting the monophyly of all infraorders, and monophyly of each of the reptant, ‘lobster’ and ‘crab’ groups, with some results supporting pleocyemate monophyly. We show that crown decapods diverged in the Late Ordovician and most crown lineages diverged in the Triassic–Jurassic, highlighting a cryptic Palaeozoic history, and post-extinction diversification. New insights into decapod relationships provide a phylogenomic window into morphology and behaviour, and a basis to rapidly and cheaply expand sampling in this economically and ecologically significant invertebrate clade.
“…Among Crustacea, which have rhabdomeric opsins (r‐opsins) typical of invertebrates, more opsins appear to be expressed in the retina than predicted based on photoreceptor sensitivities (e.g. stomatopods, Porter, Bok, Robinson, & Cronin, 2009; Porter et al., 2013; crabs, Sakamoto, Hisatomi, Tokunaga, & Eguchi, 1996; Rajkumar, Rollmann, Cook, & Layne, 2010; mysids, Frank, Porter, & Cronin, 2009; oplophorid shrimp, Wong et al., 2015; Bracken‐Grissom et al, 2020). This suggests opsins are also co‐expressed among the rhabdomeral photoreceptors of some crustaceans.…”
Diel vertical migration (DVM) of marine animals represents one of the largest migrations on our planet. Migrating fauna are subjected to a variety of light fields and environmental conditions that can have notable impacts on sensory mechanisms, including an organism's visual capabilities. Among deep‐sea migrators are oplophorid shrimp that vertically migrate hundreds of metres to feed in shallow waters at night. These species also have bioluminescent light organs that emit light during migrations to aid in camouflage. The organs have recently been shown to contain visual proteins (opsins) and genes that infer light sensitivity. Knowledge regarding the impacts of vertical migratory behaviour, and fluctuating environmental conditions, on sensory system evolution is unknown. In this study, the oplophorid Systellaspis debilis was either collected during the day from deep waters or at night from relatively shallow waters to ensure sampling across the vertical distributional range. De novo transcriptomes of light‐sensitive tissues (eyes/photophores) from the day/night specimens were sequenced and analysed to characterize opsin diversity and visual/light interaction genes. Gene expression analyses were also conducted to quantify expression differences associated with DVM. Our results revealed an expanded opsin repertoire among the shrimp and differential opsin expression that may be linked to spectral tuning during the migratory process. This study sheds light on the sensory systems of a bioluminescent invertebrate and provides additional evidence for extraocular light sensitivity. Our findings further suggest opsin co‐expression and subsequent fluctuations in opsin expression may play an important role in diversifying the visual responses of vertical migrators.
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