Structure, function and parallel evolution of the bivalve byssus, with insights from proteomes and the zebra mussel genome

Abstract

The byssus is a structure unique to bivalves. Byssal threads composed of many proteins extend like tendons from muscle cells, ending in adhesive pads that attach underwater. Crucial to settlement and metamorphosis, larvae of virtually all species are byssate. By contrast, in adults, the byssus is scattered throughout bivalves, where it has had profound effects on morphological evolution and been key to adaptive radiations of epifaunal species. I compare byssus structure and proteins in blue mussels (Mytilus), by far the best characterized, to zebra mussels (Dreissena polymorpha), in which several byssal proteins have been isolated and sequenced. By mapping the adult byssus onto a recent phylogenomic tree, I confirm its independent evolution in these and other lineages, likely parallelisms with common origins in development. While the byssus is superficially similar in Dreissena and Mytilus, in finer detail it is not, and byssal proteins are dramatically different. I used the chromosome-scale D. polymorpha genome we recently assembled to search for byssal genes and found 37 byssal loci on 10 of the 16 chromosomes. Most byssal genes are in small families, with several amino acid substitutions between paralogs. Byssal proteins of zebra mussels and related quagga mussels (D. rostriformis) are divergent, suggesting rapid evolution typical of proteins with repetitive low complexity domains. Opportunities abound for proteomic and genomic work to further our understanding of this textbook example of a marine natural material. A priority should be invasive bivalves, given the role of byssal attachment in the spread of, and ecological and economic damage caused by zebra mussels, quagga mussels and others. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.

Keywords: Dreissena polymorpha; bivalve genome; byssal threads.

Figure 1.

Phylogenetic history of the evolution of the adult byssus in bivalves. The tree is based on the phylogenomic analysis of Lemer et al. [27]. Branch lengths are proportional to genetic distances from maximum likelihood. Pie diagrams at internal and terminal nodes represent likelihoods of ancestral states based on the Mk1 model in Mesquite. Major clades are labelled in colour and minor clades are labelled within the Imparidentia. (Online version in colour.)

Figure 2.

Chromosomal locations of byssal genes in D. polymorpha. Chromosome numbers are labelled in italics. The vertical black ovals represent positions of the centromeres based on cytogenetics. Genes labelled above the chromosomes are on + strands, those below are on − strands. The yellow shaded region on chromosome 13 marks a cluster of byssal genes from three gene families.