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NATURE | VOL 403 | 17 FEBRUARY 2000 | www.nature.com 725
spirochaetes were detected in cultures fromblood samples and subcutaneous aspiratesfrom five of the infected birds in the migra-tion room. No spirochaetes were found insamples taken before that time, nor in thosefrom birds in the control room. There wasa significantly higher proportion of culture-positive birds in the migration room (fiveout of eight) than in the control room (zeroout of six) (Pearson x 245.833, 1 d.f.,P40.031; Fig. 2c). Sequencing a variablepart of the ospA gene from all cultivatedisolates confirmed that the sequences wereidentical to that of the infecting strain.
As Lyme disease Borrelia grows optimal-ly in vitro at 34–37 oC (ref. 8), the highmean body temperature of passerine birds(40.6 oC; ref. 9) was considered to rule outtheir likelihood as amplification hosts. Thebody temperature of birds is not uniform,however, either spatially or temporally, andsome parts (skin and air sacs, for example)may be at lower temperatures than the
internal organs9. Of the three different Bor-relia species causing Lyme disease, B. gariniiseems to have the highest temperature foroptimal growth10. In addition, B. garinii andB. valaisiana, which does not cause diseasein humans, are the species most often foundin birds, suggesting that these are welladapted to higher body temperatures11,12.
Our results show that migratory restless-ness in redwing thrushes can reactivate alatent Borrelia infection. As thrushes andother birds often travel great distances dur-ing migration, this reveals a new mecha-nism for facilitating the long-distancespread of Lyme disease. Ticks anywherealong a migration route can feed onmigrants with reactivated infections andbecome infected themselves, in turn passingthe disease on to other organisms.Åsa Gylfe*, Sven Bergström*, Jan Lundström†, Björn Olsen‡§*Department of Microbiology, Umeå University, SE-901 87 Umeå, Sweden†Department of Population Biology, Evolutionary Biology Center, Uppsala University,Norbyvägen 18D, SE-752 36 Uppsala, Sweden‡Department of Infectious Diseases, Umeå University, SE-901 87 Umeå, Sweden§Department of Infectious Diseases, Kalmar CountyHospital, SE-391 85 Kalmar, Swedene-mail: [email protected]. Olsen, B., Jaenson, T. G. T. & Bergström, S. Appl. Environ.
Microbiol. 61, 3082–3087 (1995).
2. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. Proc. R.
Soc. Lond. B 265, 1637–1641 (1998).
3. Apanius, V. in Stress and Behaviour (eds Møller, A. P., Milinski,
M. & Slater, P. J. B.) 133–153 (Academic, San Diego, 1998).
4. Besedovsky, H. O. & del Rey, A. Endocr. Rev. 17, 64–102 (1996).
5. Mackowiak, P. A. Rev. Infect. Dis. 6, 649–668 (1984).
6. Holberton, R. L., Parrish, J. D. & Wingfield, J. C. Auk 113,
558–564 (1996).
7. Alerstam, T. Bird Migration (Cambridge Univ. Press, 1990).
8. Barbour, A. G. Yale J. Biol. Med. 57, 521–525 (1984).
9. Welty, J. C. & Baptista, L. in The Life of Birds 119–141 (Saunders
College Publishing, New York, 1988).
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(1998).
Figure 2 Borrelia garinii infection in redwing thrushes. a, Noctur-
nal activity; b, change in body mass; and c, reactivation of infec-
tion in these birds. Photoperiod in the migration room is indicated
(bottom). Solid line/filled points, migration room; dashed line/open
points, control room. The juvenile redwing thrushes were caught
in an area where ticks and Lyme disease are rare. Each bird was
kept in an individual cage (57237250 cm) equipped with an
infrared sensor that registered all movement such as wing
whirring, fluttering and hopping. Borrelia spirochaetes were cul-
tured as described8.
Marine ecology
Do mussels take woodensteps to deep-sea vents?
Symbiont-containing mussels (Mytili-dae) are found at hydrothermal ventsand cold seeps on the ocean floor, but
it is not known whether these taxa representan ancient lineage endemic to these sur-roundings or are more recent invaders.Here we show that several small and poorlyknown mussels, commonly found onsunken wood and whale bones in the deepsea, are closely related to vent and seep taxa,and that this entire group is divergent fromother Mytilidae. Our results indicate thatvents and seeps were recently invaded by
modern mytilid taxa and suggest thatdecomposing wood and bone may haveserved as ‘steps’ for the introduction ofmytilid taxa to vents and seeps.
Symbiont-containing mussels fromhydrothermal vents and cold seeps are cur-rently placed in the recently proposedmytilid subfamily Bathymodiolinae1. Thissubfamily contains 11 species in two genera,Bathymodiolus and Tamu, all of whichobtain nutrients fixed by chemoautotrophicor methanotrophic endosymbionts har-boured inside markedly enlarged gills. Mostof these mussels are large and all are indige-nous to deep-sea hydrothermal vents orcold-water seeps2.
Chemoautotrophic endosymbionts havebeen discovered in the gills of a deep-seamytilid not typically found in vent andseep environments3. This tiny (averagelength `4 mm) mussel, Idas washingtonia,was the most abundant species (more than10,000 individuals per site) in chemo-autotrophic invertebrate communities liv-ing on four lipid-rich whale skeletons atdepths of 1,000–2,000 m on the northeastPacific slope4,5. Hydrogen sulphide, pro-duced by bacterial decomposition of lipidsin the bones, rather than vent effluents4,probably supports these communities5.
Idas washingtonia also has an unex-plained habit of wood association. Itbelongs to one of several genera of smallmussels of unknown phylogenetic affinitycommonly found on sunken wood, woodyplant materials and whale bones at depthsfrom 150 to ¤3,500 m on the sea floor6.
Surprisingly, our phylogenetic analysesbased on comparison of gene sequencesencoding ribosomal RNA (18S rRNA) indi-cate that all our samples of wood and bonemussels form a monophyletic lineage thatincludes all examined vent and seep species,but excludes members of traditional mytilidsubfamilies (Fig. 1). These analyses providestrong support for the proposed subfamilystatus of Bathymodiolinae but suggest thatthe wood- and bone-associated generaAdipicola, Idas, Myrina and Benthomodiolusshould also be included in this subfamily.
The almost identical 18S rRNAsequences within this clade (¤98.5% forthe entire group, ¤99.7% among vent andseep taxa) are consistent with recent diversi-fication and recent invasion of vent andseep environments. Although internalbranching order is not fully resolved, thebasal divergence of Benthomodiolus ligni-cola, a species observed on sunken woodand bone, receives significant bootstrapsupport7 (77–89%) by all inference meth-ods, suggesting that wood and bone associ-ation may have preceded vent and seepspecialization within this lineage.
The association of I. washingtonia withsunken wood can now be re-evaluated. Asin the case of whale bones, sulphide is a
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726 NATURE | VOL 403 | 17 FEBRUARY 2000 | www.nature.com
principal product of the bacterial degrada-tion of wood in marine environments8.Thus, Idas, through its chemosyntheticendosymbionts, may also use sulphide pro-duced by wood decomposition.
Considering their close phylogeneticrelationship and similar habitat preference,we predict that similar chemoautotrophicsymbioses exist in other wood- and bone-associated mussels. Wood and woody plantmaterials, like whale bones, sustain othertaxa known to harbour chemoautotrophicendosymbionts, including thyasirid9 and
solemyid clams10, and vestimentiferan tube-worms11. In fact, vestimentiferans have beenreported in only two non-vent or seep set-tings: a whale fall in the Santa CatalinaBasin12 and woody plant materials (bales ofsisal twine near sacks of beans and seeds) ina sunken freighter in the eastern Atlantic11:in both cases, the tubeworms occurredtogether with Idas sp.
Why should decomposing wood andbone support vent-like, chemosynthesis-based invertebrate communities whereasother organic substrates typically do not?
Both wood and bone have a high reduced-carbon content, resist consumption bydetritivores, and undergo slow and sus-tained decay. Thus, whereas opportunisticfeeders rapidly consume most types oforganic detritus in the deep sea9, large woodand bone deposits may require more thanten years to decompose4,5,9,13. Such sustaineddecomposition could be necessary to sup-port chemoautotrophy-dependent species,which may require several years to repro-duce5.
Whale falls have been proposed to act asevolutionary stepping stones for the intro-duction of chemoautotrophy-dependentinvertebrates to vent and seep environ-ments5. Sunken wood and woody plantmaterials may act similarly. These substratesare common in the deep sea14 and probablyhave been since the Carboniferous, longbefore bivalve fossils appeared at vents orseeps15. The close phylogenetic relationshipsamong wood-, bone-, vent- and seep-asso-ciated mussels are indicative of a recentcommon ancestry for vent and non-ventspecies, whereas the divergence of the entiregroup from other mytilids is indicative of along isolation from common shallow-watertaxa. These observations implicate woodand bone as historical vectors for the trans-port of mytilids to (or from) vents andseeps, and suggest a plausible role forwood- and bone-association as an evolu-tionary step towards invasion of vent andseep habitats. Daniel L. Distel*, Amy R. Baco†, Ellie Chuang‡, Wendy Morrill*, Colleen Cavanaugh‡, Craig R. Smith†*Department of Biochemistry, Microbiology, and Molecular Biology, University of Maine, Orono, Maine 04469-5735, USAe-mail: [email protected]†Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, Hawaii 96822, USA‡Biological Laboratories, Harvard University,Cambridge, Massachusetts 02138, USA1. Kenk, V. C. & Wilson, B. R. Malacologia 26, 253–271 (1985).
2. Gustafson, R. G., Turner, R. D., Lutz, R. A. & Vrijenhoek, R. C.
Malacologia 40, 63–112 (1998).
3. Deming, J. W., Reysenbach, A. L., Macko, S. A. & Smith, C. R.
J. Microsc. Res. Tech. 37, 162–170 (1997).
4. Bennett, B. A., Smith, C. R., Glaser, B. & Maybaum, H. L.
Mar. Ecol. Prog. Ser. 108, 205–223 (1994).
5. Smith, C. R., Kukert, H., Wheatcroft, R. A., Jumars, P. A. &
Deming, J. W. Nature 341, 27–28 (1989).
6. Dell, R. K. Natl Mus. NZ Rec. 3, 17–36 (1987).
7. Hillis, D. M. & Bull, J. J. Syst. Biol. 42, 182–192 (1993).
8. Leschine, S. B. Annu. Rev. Microbiol. 49, 399–426 (1995).
9. Grassle, J. F. & Morse-Porteous, L. S. Deep-Sea Res. 34,
1911–1950 (1987).
10.Reid, R. G. B. Can. J. Zool. 58, 386–393 (1980).
11.Dando, P. R., Southward, A. J. & Southward, E. C. Nature 356,
667 (1992).
12.Feldman, R. A., Shank, T. M., Black, M. B., Baco, A. R. & Smith,
C. R. Biol. Bull. 194, 116–119 (1998).
13.Dean, H. K. Malacologia 35, 21–41 (1993).
14.Wolff, T. Sarsia 1, 117–136 (1979).
15.Campbell, K. A. & Bottjer, D. J. Geology 23, 321–324 (1995).
16.Swofford, D. L. PAUP* 4.0 (Phylogenetic Analysis Using
Parsimony) (Sinauer, Sunderland, MA, 1997).
17.Distel, D. L. Mol. Phylogenet. Evol. (in the press).
Figure 1 Phylogenetic relationships among vent and non-vent mytilids. a, Taxa for which new DNA sequences for 18S RNA were exam-
ined. b, Vent-, seep-, wood- and bone-associated mussels form a clade (red), distinct from the traditional subfamilies Mytilinae (green) ,
Crenellinae (brown), Lithophagainae (purple) and Modiolinae (blue). Phylogenetic analyses used maximum likelihood (shown), maximum
parsimony and evolutionary distance algorithms16. Likelihood substitution model: HKY-85&G, with a40.865 and base frequencies and
ti:tv (1.41) estimated from the data. Heuristic searches were done with random sequence addition (100 replicates) and branch swapping
by tree-bisection–reconnection. Bootstrap proportions (percentage of 1,000 replicates) are presented (top to bottom: likelihood, distance,
parsimony). Dashes are values of *50%. The single best likelihood tree (1lnLi44,328.3) has topology identical to the best distance
and parsimony trees (319 steps) at all nodes for which bootstrap proportions are shown. Asterisk indicates significant support for mono-
phyly determined under Kishino–Hasegawa criteria (best parsimony trees constrained to non-monophyly for the indicated clade are sig-
nificantly longer (P*0.05) than best unconstrained trees). The aligned sequence set contains 23 taxa, 1,758 equally weighted sites (139
parsimony informative), aligned manually and with consideration of secondary structural information, confirmed by compensatory substi-
tutions with unalignable regions eliminated and gaps treated as missing data (GenBank accession nos AF221638–AF221648).
Hormomya domingensis and Geukensia demissa form a clade distinct from their traditional subfamilies Mytilinae and Modiolinae17.
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