A Phylogenomic Framework, Evolutionary Timeline, and Genomic Resources for Comparative Studies of Decapod Crustaceans

Abstract

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 (>86,000 bp) conserved across all lineages of Decapoda, eight times more 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 Paleozoic history, and postextinction diversification. New insights into decapod relationships provide a phylogenomic window into morphology and behavior, and a basis to rapidly and cheaply expand sampling in this economically and ecologically significant invertebrate clade. Introduction:Decapod crustaceans, broadly categorized into 'shrimp', 'lobsters', and 'crabs', are embedded in the public consciousness due to their importance as a global food source worth over $24 billion [1]. Several ornamental species are also popular in the pet trade [2,3], and some lobsters and crayfish may be promising models for cancer and aging research [4]. Furthermore, decapods are a major faunal component of a bewildering variety of global habitats, including the open ocean, seafloor vents and seeps, caves, coral reefs, mangroves and estuaries, intertidal mud and sand, freshwater streams and lakes, semi-terrestrial locations, and in symbiosis with other animals (Figure 1). Decapods have diversified over the course of 455 million years resulting in over 15,000 living and 3,000 fossil species recognized in approximately 233 families [5,6]. Despite the economic and ecological significance of the clade, higher-level phylogenetic relationships among decapods have proven recalcitrant.The majority of work is restricted to studies using morphology [7][8][9], up to nine targeted mitochondrial and nuclear genes [6,[10][11][12][13][14][15][16][17][18][19], and more recently complete mitogenomes of 13 genes [20][21][22][23][24]. Mitogenomic data can be problematic for reconstructing ancient nodes [25], and indeed, deeper relationships receive poor support [24]. As part of a larger analysis, decapods were included in a recent transcriptomic study [26], but with limited taxon sampling within the order. This plurality of results, several based on the same underlying data [25], have reported conflicting deep relationshi...

Masters of communication: The brain of the banded cleaner shrimp Stenopus hispidus (Olivier, 1811) with an emphasis on sensory processing areas

“…In summary, the neural architecture of S. hispidus supports its phylogenetic position according to recent phylogenomic analyses Figure a (Schwentner et al, ; Wolfe et al, ), since it shares more similarities with the caridean brain than with its dendrobranchiate relatives.…”

“…The phylogenetic position of Stenopodidea within Malacostraca is uncertain with regard to the Decapoda, because stenopodid shrimps share characters of euphausiids such as the sperm morphology but also characters (referring the internal and external morphology, larval development and behavior) indicating a closer relationship to reptants (reviewed in Goy, ). Two recent phylogenomic analyses (Schwentner et al, ; Wolfe et al, ) concordantly consider Stenopodidea to be the sister‐group to all other Caridea (see phylogram in Figure a). The first neuroanatomical description of its central brain was provided by Sandeman and coworkers (Sandeman, Scholtz, & Sandeman, ) and information on the visual neuropils and the neuropils of the lateral protocerebrum (lPC) (those parts of the brain situated within the eyestalk) was added by Sullivan and Beltz () (reviewed in Sandeman, Kenning, & Harzsch, ) and recently by Wolff, Thoen, Marshall, Sayre, and Strausfeld ().…”

The late blooming amphipods: global change promoted post-Jurassic ecological radiation despite Palaeozoic origin

“…suggest that a phylogenomic approach could prove invaluable for a better understanding of amphipod 466 evolution, as evidenced in a recent study on decapod crustaceans (Wolfe et al 2019). However, any 467…”

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

“…therein). Moreover, most studies dealing with phylogenetic analyses have recovered a paraphyletic podotreme grade (e.g., Ahyong et al, 2007;Scholtz and McLay, 2009;Karasawa et al, 2011;Tsang et al, 2014;Luque et al, 2019a;Wolfe et al, 2019). In addition, the distribution of visual systems across brachyuran clades is poorly understood.…”