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

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’.

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Deepwater population structure and reproductive state of quagga mussels (Dreissena bugensis) in Lake Erie

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f97-151 ◽

1997 ◽

Vol 54 (10) ◽

pp. 2428-2433 ◽

Cited By ~ 40

Author(s):

S L Roe ◽

H J MacIsaac

Keyword(s):

Population Structure ◽

Dreissena Polymorpha ◽

Lake Erie ◽

Soft Tissues ◽

Gonadal Development ◽

Zebra Mussels ◽

Reproductive State ◽

Dreissena Bugensis ◽

Frequency Distributions ◽

Quagga Mussels

Quagga mussel (Dreissena bugensis) population structure and reproductive status were assessed at deepwater (37 and 55 m) sites in eastern Lake Erie during July 1996. Mussels occupied ~70% of soft substrates at 37-m sites and between 63 and 90% at 55-m sites. Shell length and dry mass frequency distributions were similar at both sites, although recruits <<= 5 mm comprised a larger proportion of the population at the deeper site. The population surveyed here allocated disproportionately less mass to shell and more to soft tissues relative to zebra mussels (Dreissena polymorpha) from shallow-water sites in eastern Lake Erie and from Lake St. Clair. The population at 55 m was slightly skewed toward male mussels (58%). Female mussels that were examined for reproductive state contained mature oocytes (80%) or had spent gonads (20%). Because water temperature at the site was only 4.8°C, this survey provides the first evidence of gonadal development and spawning by quagga mussels at low temperature. These findings contrast with most reports of spawning by congeneric zebra mussels at temperatures >=>12°C but are consistent with distributions of the species in different basins of the lake.

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Physiological energetics of Lake Erie dreissenid mussels: a basis for the displacement of Dreissena polymorpha by Dreissena bugensis

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f03-005 ◽

2003 ◽

Vol 60 (2) ◽

pp. 126-134 ◽

Cited By ~ 89

Author(s):

Ann Stoeckmann

Keyword(s):

Body Mass ◽

Dreissena Polymorpha ◽

Lake Erie ◽

Shell Growth ◽

Zebra Mussels ◽

Sympatric Populations ◽

Dreissena Bugensis ◽

Quagga Mussels ◽

Respiration Rates ◽

Western Lake

I measured respiration, shell growth, body mass, and reproduction in sympatric populations of zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels in western Lake Erie to determine if the species differ in physiological parameters and if any differences provide an explanation for the recent displacement of zebra mussels by quagga mussels. Between May and August, I measured respiration (1998), shell growth of marked mussels suspended in cages in the lake (19992000), soft body mass and mass of gametes released (19982001), and the number of gametes released by individual mussels (1999). Quagga mussels had lower respiration rates and greater shell growth and body mass. There was no difference in the percentage of spawning mussels or the number of sperm released by individuals, but zebra mussels generally released more eggs and a greater mass of gametes than did quagga mussels. Similar reproduction at a lower body mass indicates that zebra mussels devote a greater proportion of body tissue to reproduction. Lower respiration rates and larger size give quagga mussels a competitive advantage and may explain their displacement of zebra mussels.

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Physiological and Taxonomic Separation of Two Dreissenid Mussels in the Laurentian Great Lakes

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f93-253 ◽

1993 ◽

Vol 50 (11) ◽

pp. 2294-2297 ◽

Cited By ~ 25

Author(s):

S. Domm ◽

R.W. McCauley ◽

E. Kott ◽

J. D. Ackerman

Keyword(s):

Dreissena Polymorpha ◽

Morphological Characteristics ◽

Zebra Mussels ◽

Shell Morphology ◽

Survival Times ◽

Quagga Mussels ◽

Average Survival ◽

Thermal Histories ◽

Allozyme Loci ◽

Ecological Differences

Physiological techniques were used to separate two related Dreissena species initially established by electrophoretic and morphological characteristics (May and Marsden. 1992. Can. J. Fish. Aquat. Sci. 49: 1501–1506). Samples of zebra mussels (Dreissena polymorpha) and "quagga" mussels (provisionally either Dreissena polymorpha andrusovi or Dreissena rostriformis bugensis) of the same size growing side by side were collected in Lake Erie, thereby ensuring that they had identical thermal histories. Upper lethal temperatures of zebra mussels were significantly higher than those of quagga mussels. The critical thermal maxima of zebra mussels acclimatized at 20 °C were half a degree higher than those of quagga mussels. The average survival times of zebra mussels held at a constant lethal temperature were also significantly longer. These results indicate that in addition to differences in allozyme loci and shell morphology, these two dreissenids may be distinguished by important physiological differences in their thermal resistance; moreover, there may be important ecological differences associated with the different species of dreissenids in North America.

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Sources of bias in the use of shell fragments to estimate the size of zebra and quagga mussels (Dreissena polymorpha and Dreissena bugensis)

Canadian Journal of Zoology ◽

10.1139/z99-042 ◽

1999 ◽

Vol 77 (6) ◽

pp. 910-916 ◽

Cited By ~ 3

Author(s):

Jeremy S Mitchell ◽

Robert C Bailey ◽

Richard W Knapton

Keyword(s):

Shell Length ◽

Dreissena Polymorpha ◽

Zebra Mussels ◽

Shell Morphology ◽

Selective Predation ◽

Dreissena Bugensis ◽

Quagga Mussels ◽

Length Relationship ◽

Mussel Shells ◽

Study Sites

Several researchers have examined size-selective predation on dreissenid mussels by first measuring septa from crushed mussel shells found in predators' gastrointestinal tracts and then using a regression of septum length on shell length to infer the size of consumed mussels. We examine three assumptions made when using this approach: (1) that the shell length : septum length relationship is site-independent within the study area, (2) where both zebra mussels (Dreissena polymorpha) and quagga mussels (Dreissena bugensis) are present, that the shell length : septum length relationship is the same for both mussel species, and (3) that the predator foraged exclusively at the site of collection. We collected mussels at 6 sites along an 8-km stretch of Lake Erie shoreline and found that the shell length : septum length relationship varied significantly both among sites and between zebra mussels and quagga mussels. We then compared the regression for quagga mussels at one of these sites with that for intact valves of mussels taken from scaup (Aythya marila, Aythya affinis) collected at the site. Although ice cover at the time of collection restricted scaup to the site while foraging within the study area, regressions were again significantly different, i.e., scaup had been foraging elsewhere. Our results indicate that for at least some study sites, the use of septa to estimate dreissenid mussel size is not appropriate. However, when intact valves are found in a predator, variation in shell morphology can help to confirm or exclude possible foraging locales.

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Comparative growth and feeding in zebra and quagga mussels (Dreissena polymorpha and Dreissena bugensis): implications for North American lakes

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f02-043 ◽

2002 ◽

Vol 59 (4) ◽

pp. 680-694 ◽

Cited By ~ 118

Author(s):

Brad S Baldwin ◽

Marilyn S Mayer ◽

Jeffrey Dayton ◽

Nancy Pau ◽

Johanna Mendilla ◽

...

Keyword(s):

Dreissena Polymorpha ◽

Assimilation Efficiency ◽

Zebra Mussels ◽

Functional Responses ◽

Dreissena Bugensis ◽

Chl A ◽

Quagga Mussels ◽

High Productivity ◽

Per Capita ◽

Lower Biomass

In laboratory experiments, quagga mussels (Dreissena bugensis) survived as well as zebra mussels (Dreissena polymorpha) and equaled or exceeded their growth rate (3 to 242% change in wet mass) when reared at 6 or 23°C and fed natural seston or Chlamydomonas at food levels ranging from 0.057.4 µg·L1 chlorophyll a (chl a). Superior growth of quagga mussels was most pronounced at low food levels. We found no significant differences in per capita clearance rates (CR), functional responses, or feeding behavior between zebra and quagga mussels fed Chlamydomonas, Nannochloris, or mixed suspensions of Nannochloris and clay. Per capita CR ranged from 0.018 to 0.402 L·mussel1·h1 for zebra mussels and from 0.010 to 0.407 L·mussel1·h1 for quagga mussels. Because quagga mussels had more biomass per unit shell length, we found lower biomass-specific CR for quagga mussels. When fed natural seston, zebra and quagga mussels could selectively reject inorganic material and at the lowest seston level the assimilation efficiency of quagga mussels (81%) was significantly higher than that of zebra mussels (63%). Our experiments suggest that quagga mussels can survive, grow, and feed as well or better than zebra mussels in epilimnetic waters with either low or high productivity.

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