Comparative genomics of the coconut crab and other decapod crustaceans: exploring the molecular basis of terrestrial adaptation

Abstract

Background The complex life cycle of the coconut crab, Birgus latro, begins when an obligate terrestrial adult female visits the intertidal to hatch zoea larvae into the surf. After drifting for several weeks in the ocean, the post-larval glaucothoes settle in the shallow subtidal zone, undergo metamorphosis, and the early juveniles then subsequently make their way to land where they undergo further physiological changes that prevent them from ever entering the sea again. Here, we sequenced, assembled and analyzed the coconut crab genome to shed light on its adaptation to terrestrial life. For comparison, we also assembled the genomes of the long-tailed marine-living ornate spiny lobster, Panulirus ornatus, and the short-tailed marine-living red king crab, Paralithodes camtschaticus. Our selection of the latter two organisms furthermore allowed us to explore parallel evolution of the crab-like form in anomurans. Results All three assembled genomes are large, repeat-rich and AT-rich. Functional analysis reveals that the coconut crab has undergone proliferation of genes involved in the visual, respiratory, olfactory and cytoskeletal systems. Given that the coconut crab has atypical mitochondrial DNA compared to other anomurans, we argue that an abundance of kif22 and other significantly proliferated genes annotated with mitochondrial and microtubule functions, point to unique mechanisms involved in providing cellular energy via nuclear protein-coding genes supplementing mitochondrial and microtubule function. We furthermore detected in the coconut crab a significantly proliferated HOX gene, caudal, that has been associated with posterior development in Drosophila, but we could not definitively associate this gene with carcinization in the Anomura since it is also significantly proliferated in the ornate spiny lobster. However, a cuticle-associated coatomer gene, gammacop, that is significantly proliferated in the coconut crab, may play a role in hardening of the adult coconut crab abdomen in order to mitigate desiccation in terrestrial environments. Conclusion The abundance of genomic features in the three assembled genomes serve as a source of hypotheses for future studies of anomuran environmental adaptations such as shell-utilization, perception of visual and olfactory cues in terrestrial environments, and cuticle sclerotization. We hypothesize that the coconut crab exhibits gene proliferation in lieu of alternative splicing as a terrestrial adaptation mechanism and propose life-stage transcriptomic assays to test this hypothesis.

A chromosome‐level genome of Portunus trituberculatus provides insights into its evolution, salinity adaptation and sex determination

“…Markers between linkage groups and scaffolds exhibited fine collinearities, suggesting that our assembly was of high continuity and high accuracy (Figure 1). The assembly statistics of the crab genome are comparable to, or better than, those previously published crab genomes, like E. sinensis (scaffold N50: 17.13 Mb) (Cui et al, 2021) and Birgus latro (scaffold N50: 6.35 Kb) (Veldsman et al, 2021). However, it was not as good as the previous published genome of the crab (contig N50: 4,109.06 kb and scaffold N50: 4,121.42 kb) .…”

“…The assembly statistics of the crab genome are comparable to, or better than, those previously published crab genomes, like E . sinensis (scaffold N50: 17.13 Mb) (Cui et al, 2021) and Birgus latro (scaffold N50: 6.35 Kb) (Veldsman et al, 2021). However, it was not as good as the previous published genome of the crab (contig N50: 4,109.06 kb and scaffold N50: 4,121.42 kb) (Tang, Zhang, et al, 2020).…”

Recent advances in crustacean genomics and their potential application in aquaculture

“…Among them, the American lobster Homarus americanus has the fewest predicted genes (12,598), whereas the lobster Panulirus ornatus has the most (99,127). 67,68 Gene prediction appears to be more accurate following the improvement of genome assembly quality and the development of gene prediction methods. The number of protein-coding genes in Daphnia pulex has decreased from 30,907 in the first version of the genome to 27,985 in the latest version (PRJNA794129).…”

“…67 Terrestrial adaptation: There is a limited number of terrestrial crustacean species, with the coconut crab (Birgus latro), land-hopper (Platorchestia hallaensis), sand-hopper (Trinorchestia longiramus) and pilllbug Armadillidium being some of the most representative examples. 62,68,79,80 The expansion of genes involved in visual, respiratory, olfactory, and cytoskeletal systems has been identified to play important roles in the terrestrial adaptation of coconut crab. 68 Moreover, the expansion of gene families involved in homeostatic processes and ionic and osmotic stress tolerance has been found to contribute to the terrestrial adaptation of the sand-hopper.…”

“…62,68,79,80 The expansion of genes involved in visual, respiratory, olfactory, and cytoskeletal systems has been identified to play important roles in the terrestrial adaptation of coconut crab. 68 Moreover, the expansion of gene families involved in homeostatic processes and ionic and osmotic stress tolerance has been found to contribute to the terrestrial adaptation of the sand-hopper. 80 Extreme environment adaptation: Some crustaceans inhabit extreme environmental conditions, such as those occurring in the deep sea (e.g., Bathynomus jamesi), as well as extreme salinity and complete anoxia (e.g., Artemia spp.).…”