Shift in symbiotic lifestyle as the major process shaping the evolution of pea crabs (Decapoda: Brachyura: Pinnotheroidea)

Abstract

The pea crabs, superfamily Pinnotheroidea, are exceptional among brachyuran crabs in their diverse symbiotic associations involving both inquilinism and protective symbiosis. While this group presents a rare opportunity for evolutionary comparative study of host switching and morphological evolution in marine macroinvertebrates, previous phylogenetic studies have been focused on systematics. Here, we reconstructed the most extensive phylogeny of Pinnotheroidea based on two mitochondrial and six nuclear markers, with the aim of elucidating the host switching pathways and the correlation between symbiotic lifestyles and selected morphological adaptations. Ancestral state reconstruction of host association revealed a monophyletic origin of symbiosis in the form of inquilinism. Subsequent shifts in microhabitat preference for burrows or worm tubes, and the move to protective symbiosis, primarily in the switch to mollusc endosymbiosis, contributed to radiation in Pinnotheridae. Further parallel colonisations of echinoderms and tunicates occurred but did not lead to extensive diversification, except in the Clypeasterophilus + Dissodactylus lineage, which experienced a unique switch to echinoderm ectosymbiosis. The evolution of the third maxillipeds, carapace shape and ambulatory pereiopods suggests a rather strong coupling with the symbiotic lifestyle (whether inquilinism or protective symbiosis). Phenotypic diversity of these characters was higher among species engaged in protective symbiosis, with convergence in form (or function) among those sharing the same host affiliation. Species having different host affiliations or symbiotic lifestyles might also exhibit convergence in the form of the three morphological traits, suggesting a common adaptive value of the specialisations. Pinnotherid crabs overall exhibited a lower trait diversity than the also symbiotic palaemonid shrimps with comparable species diversity. This may plausibly be attributed to differences in potential for morphological modification to serve additional functions among the traits analysed in the two groups, the less frequent host switching and the less diverse host affiliations, and thus a less complicated evolutionary history in pinnotherids.