Philodina spp. from Scotia Marsh, Arizona
Current Research Projects
Speciation in an Ancient Asexual
Organism
One of the major problems of biology is why most organisms
reproduce sexually at least part of the time. Theory and some experimental
evidence suggests that the loss of sexual reproduction should reduce the
effectiveness natural selection. Asexual lineages should accumulate detrimental
mutations, leading to extinction. They should also have difficulty retaining
and fixing advantageous mutations, which would make it difficult to adapt
to new environments and speciate. In fact the definition of species in asexual
organisms is controversial, since the "biological" species definition
cannot be applied. We are studying the long-term consequences of the loss
of asexual reproduction, and the preliminary results are exciting! The bdelloid
rotifers are a widespread group of freshwater invertebrates which have been
reproducing asexually for at least 40 million years and undergone substantial
differentiation into species differing in morphology, habitat, and behavior.
(See the movie at BdelloidMovieShort.mov.)
We are collecting bdelloid rotifers and amplifying and
sequencing a fragment of the mitochondrial coxI gene from each isolate.
Together with Tim Barraclough and Austin Burt (Barraclough,
Birky, and Burt 2003), we used basic population genetic theory to show
that asexual organisms, like sexual organisms, should fall into clusters
representing independently evolving lineages. We devised a new species concept,
the Evolutionary Genetic Species Concept, for asexuals which describes clusters
that are comparable to biological species in sexual organisms. We also devised
a species criterion, the 4-time rule, that can be used to identify such
asexual species from DNA sequences of small samples. This work is described
in a preliminary paper (Birky
et al. 05) and a Powerpoint presentation (EEBSeminar).
The paper also describes evidence that some species are adapted to different
ecological niches. Analyses of the same DNA sequences used for phylogenetic
analysis found that anciently asexual bdelloid rotifer lineage showed about
the same intensity of selection (measured by Ka/Ks) as their sexual sister
group, the monogonont rotifers.
Our Evolutionary Genetic Species Concept and criterion
appear to be applicable to other asexual organisms, including the eukaryotic
protist Giardia and at least some bacterial species.
Natural Selection and Sex
Now that we can identify species in bdelloid rotifers,
we can compare them with their sexual relatives, the monogonont rotifers,
to study the volutionary advantage of sex. The great geneticist H. J. Muller
showed that asexual organisms should accumulate detrimental mutations due
to random drift, more so than their sexual relatives. We can test this using
the cox1 gene sequences that we use for phylogenetic analysis. If
the asexual bdelloids accumulate more detrimental mutations than the sexual
monogononts, this should be reflected in a higher ratio of nonsynonymous
to synonymous substitutions (Ka/Ks) along the long evolutionary branches
connecting species to their ancestors. Matt Meselson's lab showed that this
effect was not seen in nuclear genes, and our preliminary work verified
this with the cox1 gene in a large sample of bdelloids. With collaborator
(and former graduate student) Heather Maughan at the University of British
Columbia, we are extending this analysis to a largr sample of bdelloids
and monogononts. The results to date verify that Ka/Ks is similar in the
asexual and sexual groups. Now the big puzzle is how bdelloids have managed
to escape the ratchet.
Genetic Diversity and Sex
We have also found that the nucleotide diversity of the
cox1 gene in bdelloids is similar to that of other invertebrates,
both macroscopic and microscopic. This suggests that the effective population
size is modest, even though the census population size is immense. Evidently
bdelloids have not escaped Muller's ratchet by having extremely large effective
population sizes.
Frozen Rotifers
Bdelloid rotifers are remarkably tough. Among other things,
they withstand dessication and disperse by blowing around in the wind when
dessicated. Moreover, they have been found in temporary waters in Antarctica
and on the top of 12,000-foot mountains in the U.S. Former undergrad student
Julia Perry found that bdelloids also survive freezing at -80°C, in
culture medium without cryoprotectants or any other special treatment. Undergrad
Aki Sugi has found good survival and reproduction after freezing for more
than 2.5 years. Remarkably, they do not survive freezing at -20°, perhaps
because it is too slow.
Testing the "Everything is Everywhere"
Hypothesis
We are now able to test an important hypothesis in biogeography,
the Everything is Everywhere hypothesis. This hypothesis says that microscopic
organisms have such large population sizes that every species can be found
everywhere, although the local environment determines whether a species
thrives at a particular location. Some of the data favoring this hypothesis
are based on species identified by morphology, which is often a misleading
criterion, especially for microscopic organisms. Our preliminary data suggest
that although many or most bdelloid rotifer species disperse broadly and
rapidly, not all do so and most of the species we find in the U.S. are not
found in collections from Europe, Africa, and elsewhere. Currently undergrduate
student Chris Wisneiwski is working on methods of isolating bdelloids from
soil samples.
Rotifer Systematics
Our collection includes a number of new species. We have
four species of Abrochtha, of which at least three are new; we are
collaborating with Claudia Ricci, Giulio Melone, and Diego Fontaneto of
the University of Milan to describe the new species. Two of them are cryptic
species, distinguishable by genotype but not be phenotype.
Link to the labs of collaborator Claudia Ricci's
web site at the University of Milan: http://users.unimi.it/ricci/rotifer.htm
DNA Barcoding
DNA barcoding is the use of DNA sequences to identify specimens
to species, and to discover new species. It has previously been applied
only to sexual organisms and primarily uses the mitochondrial cox1
gene. These efforts are controversial because mitochondral gene phylogenies
do not necessarily agree with nuclear gene phylogenies. However, this objection
does not apply to asexual organisms in which all genes are completely linked
and mitochondrial genes necessarily have the same phylogenetic history as
nuclear genes and individuals. Our theoretical model of speciation and our
application to bdelloid rotifers and bacteria shows that barcoding works
well with asexual and clonal organisms, which includes many parasites and
microorganisms of medical and agricultural importance.
DNA barcode of Philodina roseola; each
color represents a different base in the cox1 sequence.
Link to the Barcode Blog: http://phe.rockefeller.edu/barcode/blog/
Folding the Bdelloid ITS Sequences
Lea Gemmel is studying the folding of the nuclear ITS1
RNA, with the aim of using the folding structure to improve the alignment
of this region. We can then compare phylogenetic trees produce with the
5.8S-ITS1 sequence to the trees produced with mitochndrial genes. Preliminary
results show some discrepancies which may be due to the presence of divergent
paralogous copies of this region in bdelloids.
Some Representative Publications
Birky, C. William, Jr., and John J. Gilbert, 1971 Parthenogenesis in
rotifers: the control of sexual and asexual reproduction. Am. Zoologist
11:245-266.
Birky, C. William, Jr.,1973 On the origin of mitochondrial mutants: Evidence
for intracellular selection of mitochondria in the origin of antibiotic-resistant
cells in yeast. Genetics 74:421-432. Birky73IntracellSelectMito.pdf
Thrailkill, Kathryn M., C. William Birky, Jr., Gudrun Lückemann,
and Klaus Wolf, 1980 Intracellular population genetics: Evidence for random
drift of mitochondrial allele frequencies in Saccharomyces cerevisiae
and Schizosaccharomyces pombe. Genetics 96:237-262. Thrailkill80MitoDrift.pdf
Birky, C. William, Jr., Karen P. VanWinkle-Swift, Barbara B. Sears, John
E. Boynton, and Nicholas W. Gillham, 1981 Frequency distributions for chloroplast
genes in Chlamydomonas zygote clones: Evidence for random drift.
Plasmid 6:173-192. Birky81ChlamyCpRandomDrift.pdf
Birky, C. William, Jr., Takeo Maruyama, and Paul Fuerst, 1983 An approach
to population and evolutionary genetic theory for genes in mitochondria
and chloroplasts, and some results. Genetics 103:513-527. Birky83OrgPopGenTheory1.pdf
Banks, Jo Ann, and C. William Birky, Jr., 1985 Chloroplast DNA diversity
is low in a wild plant, Lupinus texensis. Proc. Nat. Acad. Sci. USA
82:6950-6954. Banks85LupineCpDiversity.pdf
Birky, C. William, Jr., and J. Bruce Walsh, 1988 Effects of linkage on
rates of molecular evolution. Proc. Nat. Acad. Sci. USA 85:6414-6418.
Birky88Linkage&EvolRates.pdf
Birky, C. William, Jr., Paul Fuerst, and Takeo Maruyama, 1989 Organelle
gene diversity under migration, mutation, and drift: Equilibrium expectations,
approach to equilibrium, effects of heteroplasmic cells, and comparison
to nuclear genes. Genetics 121:613-627. Birky89OrgPopGenTheory2.pdf
Birky, C. William, Jr., 1995 Uniparental inheritance of mitochondria
and chloroplast genes: mechanisms and evolution. Proc. Nat. Acad. Sci.
USA 92:11331-11338. Birky95UPI.pdf
Rumpf, Robert, Dawne Vernon, David Schreiber, and C. William Birky, Jr.,
1996 Evolutionary consequences of the loss of photosynthesis in Chlamydomonadaceae:
Phylogenetic analysis of Rrn18 (18S rDNA) in 13 Polytoma strains
(Chlorophyta). J. Phycol. 32:119-126. Rumpf96PolytomaPhylogeny.pdf
Birky, C. William, Jr., 1996 Heterozygosity, heteromorphy, and phylogenetic
trees in asexual eukaryotes. Genetics 144:427-437. Birky96Heterozygosity.pdf
Birky, C. William, Jr., 1999 An even broader perspective on the evolution
of sex. J. Evol. Biol. 12:1013-1016. Birky99BroaderPerspective.pdf
Birky, C. William, Jr., 2001 The inheritance of genes in mitochondria
and chloroplasts: Laws, mechanisms, and models. Annu. Rev. Genet.
35:125-148. Birky01AnnRevGenet.pdf
Vernon, Dawne, Robin Gutell, Jaime Cannone, Robert Rumpf, and C. William
Birky, Jr., 2001. Accelerated evolution of functional plastid rRNA and elongation
factor genes due to reduced protein synthetic load after the loss of photosynthesis
in the chlorophyte alga Polytoma.. Mol. Biol. Evol. 18:1810-1822.
Vernon01PolyRates.pdf
Lizhi Yu, C.. William Birky, Jr., and Rodney D. Adam, 2002. The two nuclei
of Giardia each have complete copies of the genome as demonstrated
by fluorescence in situ hybridization. Eukaryotic Cell 1:191-199.
Yu02Giardia.pdf
Maughan, H., C. W. Birky,Jr, W. L. Nicholson, W. D. Rosenzweig, and R.
H. Vreeland, 2002.The paradox of the "ancient' bacterium which contains
"modern" protein-coding genes. Molecular Biology and Evolution
19:1637-1639. Maughan02BacillusPermians.pdf
Barraclough, Timothy G., C. William Birky, Jr., and Austin Burt, 2003
Diversification in sexual and asexual organisms. Evolution 57:2166-2172.
BarraBirkyBurt2003.pdf
Birky, C. William, Jr. (2004) Bdelloid rotifers revisited. Proceedings
of the National Academy of Sciences USA 101:2651-2652. Birky04BdelloidsRevisited.pdf
Birky, C. William, Jr. (2004) Sex: Is Giardia doing it in the dark?.
Current Biology 15:R56-R56. Birky05SexInGiardia?.pdf
Maughan , Heather (2004) Stochastic processes influence stationary-phase
decisions in Bacillus subtilis. Journal of Bacteriology 186:2212-2214.
Maughan04StchstcVariatn&Sel.pdf
Birky, C. William, Jr., Cynthia Wolf, Heather Maughan, Linnea Herbertson,
Elena Henry (2005) Speciation and selection without sex. Hydrobiologia
546:29-45. Birky05RotiferaX.pdf
Go to Research History
for a summary of Bill's previous research. Go to Publications
for a complete list of Bill's papers.
Some files are in pdf format. You can view
them with the Acrobat Reader software, available free at http://www.adobe.com.
|
