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Divergent Gene Copies in the Asexual Class Bdelloidea (Rotifera) Separated Before the Bdelloid Radiation Or Within Bdelloid Families

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Divergent Gene Copies in the Asexual Class Bdelloidea (Rotifera) Separated Before the Bdelloid Radiation Or Within Bdelloid Families Divergent gene copies in the asexual class Bdelloidea (Rotifera) separated before the bdelloid radiation or within bdelloid families David B. Mark Welch†‡, Michael P. Cummings†§, David M. Hillis¶, and Matthew Meselson†ʈ †Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biology Laboratory, Woods Hole, MA 02543; ¶Section of Integrative Biology and Center for Computational Biology and Bioinformatics, University of Texas, Austin, TX 78712; and ʈDepartment of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138 Contributed by Matthew Meselson, October 15, 2003 Rotifers of the asexual class Bdelloidea are unusual in possessing can produce a more robust phylogeny, we conducted new two or more divergent copies of every gene that has been exam- analyses (initiated by D.M.H.). We find that phylogenetic anal- ined. Phylogenetic analysis of the heat-shock gene hsp82 and the ysis of the available data cannot discriminate between gene trees TATA-box-binding protein gene tbp in multiple bdelloid species that differ in the placement of the root of hsp82 and of tbp suggested that for each gene, each copy belonged to one of two bdelloid gene divergence, thereby leaving it unclear whether the lineages that began to diverge before the bdelloid radiation. Such most divergent gene copies separated before the bdelloid radi- gene trees are consistent with the two lineages having descended ation or within bdelloid families. from former alleles that began to diverge after meiotic segregation ceased or from subgenomes of an alloploid ancestor of the bdel- Materials and Methods loids. However, the original analyses of bdelloid gene-copy diver- Sequences Examined. Sequences and alignments have been reported gence used only a single outgroup species and were based on (1, 2) and are available from D.B.M.W. or the rotifer biology parsimony and neighbor joining. We have now used maximum database Wheelbase (http:͞͞jbpc.mbl.edu͞wheelbase). GenBank likelihood and Bayesian inference methods and, for hsp82, multiple accession numbers are AF143849–AF143858, AF249985– outgroups in an attempt to produce more robust gene trees. Here AF250004, AF375825, and AF375826. The species examined were we report that the available data do not unambiguously discrim- Seisonida: Seison nebaliae Grube 1859; Acanthocephala: Monili- inate between gene trees that root the origin of hsp82 and tbp formis moniliformis (Bremser 1811), Oligacanthorhynchus tortuosa copy divergence before the bdelloid radiation and those which (Leidy 1850), and Oncicola sp. (Archiacanthocephala); Monogo- indicate that the gene copies began to diverge within bdelloid nonta: Brachionus plicatilis Mueller 1786 strain AUS, Brachionus families. The remarkable presence of multiple diverged gene copies calyciflorus Pallas 1766 (Ploima, Brachionidae), Eosphora ehren- in individual genomes is nevertheless consistent with the loss of bergi Weber 1918 (Ploima, Notommatidae), and Sinantherina so- sex in an ancient ancestor of bdelloids. cialis (Linnaeus 1758) (Flosculariacea, Flosculariidae); and Bdel- loidea: Philodina roseola Ehrenberg 1832, Macrotrachela f a diploid lineage abandons the cycle of meiosis and syngamy quadricornifera (Milne 1886) (Philodinida, Philodinidae), Habro- Ithat characterizes sexual reproduction and engages in no other trocha constricta (Dujardin 1841) (Philodinida, Habrotrochidae), form of lateral gene transfer, former alleles will no longer and Adineta vaga (Davis 1873) (Adinetida, Adinetidae). segregate and, because of the cessation of genetic drift, will no longer be kept nearly identical. Conversion, mitotic crossing ML Analysis of hsp82. MODELTEST (3) was used to determine over, and nondisjunction then will be the only processes oppos- appropriate nucleotide-based evolutionary models. Three parti- ing the mutational accumulation of neutral divergence between tions of the data were considered: all nucleotides, codon first and sequences at loci of former alleles in individual genomes. In such second positions, and codon third positions. For each partition, the an asexual system, divergence between such sequences will best model by the Akaike Information Criterion was General Time reflect the time since they last experienced one of these pro- Reversible with a gamma-shape parameter and proportion of cesses. If there are particular cases in which descendants of invariant sites to estimate rate heterogeneity. The alpha-shape former alleles have escaped these processes, their divergence will parameter of the gamma distribution and the percent of invariant reflect the time since sexual reproduction ceased. sites for the three partitions of the data set were 1.27 and 0.35, 0.32 Genomes of rotifers of the asexual class Bdelloidea are unusual and 0, and 2.51 and 0, respectively. Likelihood ratio tests showed a in that they possess two or more divergent copies of every gene that simpler model (Tajima–Nei) to be sufficient for all nucleotides and has been examined and lack closely similar copies (ref. 1 and for codon third positions; this model produced the same topology D.B.M.W. and M.M., unpublished data). Previously (1), two of us with slightly lower bootstrap support (data not shown). presented gene trees of the heat-shock gene hsp82 and the TATA- PAUP* 4.0b10 (4) was used to find the best ML tree by using a box-binding protein gene tbp that were consistent with the separa- heuristic search with tree bisection–reconnection and 1,000 tion of the most divergent copies of both genes before the bdelloid random-addition-sequence replications. Bootstrap values were radiation and after the separation of bdelloids from their sister generated in heuristic searches with 1,000 bootstrapped data sets taxon, the facultatively sexual monogonont rotifers (for hsp82, see and 10 random-addition-sequence replications for each boot- Fig. 1A). Although the possibility was cited that these copies could strap replicate. represent ancient duplications or components of an ancient polyploid, the time of their apparent separation was seen as Abbreviation: ML, maximum likelihood. consistent with their descent from a pair of former alleles. ‡To whom correspondence should be addressed at: Josephine Bay Paul Center for Com- The original trees were generated by parsimony and neighbor parative Molecular Biology and Evolution, Marine Biological Laboratory, 7 MBL Street, joining based on 4-fold degenerate codon positions and used a Woods Hole, MA 02543. E-mail: [email protected]. single outgroup to root the bdelloid gene copies. Because §Present address: Center for Bioinformatics and Computational Biology, University of multiple outgroups, more sophisticated evolutionary models, Maryland, College Park, MD 20742. and maximum likelihood (ML) and Bayesian inference methods © 2004 by The National Academy of Sciences of the USA 1622–1625 ͉ PNAS ͉ February 10, 2004 ͉ vol. 101 ͉ no. 6 www.pnas.org͞cgi͞doi͞10.1073͞pnas.2136686100 Downloaded by guest on September 27, 2021 EVOLUTION Fig. 1. Three gene trees of hsp82 in Rotifera. Monogononts, acanthocephalans, and the seisonid are described in ref. 1; bdelloids and the notation of bdelloid gene copies are described in ref. 2. (A) The tree presented in ref. 1. Branch lengths are proportional to the number of changes by maximum parsimony, with support for clades shown as a percent of 1,000 bootstrap replicates by maximum parsimony (above) and neighbor joining of a Kimura two-parameter distance matrix (below).(B) The tree found by a heuristic ML search using a nucleotide model of all positions. Branch lengths are proportional to the inferred number of substitutions, with support for clades shown as percent of bootstrap support (above) and posterior probability (below). Support for Philodinidae ranged from 71% to 76% of bootstrap replicates and from 91% to 97% posterior probability using various models of nucleotide substitution; the same rooting of bdelloid sequences is obtained when only codon third positions are used. (C) The tree found by a heuristic ML search using a nucleotide model of codon first and second positions. Branch lengths are proportional to the inferred number of substitutions, with support for clades shown as percent of bootstrap support (above) and posterior probability (below). The same rooting of bdelloid sequences is found when a codon-based model is used with ML. For codon-based ML, the codeml program in PAML 3.13a (5) by likelihood ratio tests and Akaike Information Criterion, was was used to determine the ML score for the tree in Fig. 1B under codon equilibrium frequencies estimated as free parameters a variety of models. The most appropriate model, as determined from the existing codon frequencies (60 parameters) and non- Mark Welch et al. PNAS ͉ February 10, 2004 ͉ vol. 101 ͉ no. 6 ͉ 1623 Downloaded by guest on September 27, 2021 Table 1. Comparison of tree alternatives for hsp82 Criteria Model Tree BP PP KH SH Nucleotide model, all positions B 0.732 (0.004) 0.900 (0.000) 0.729 (0.004) 0.729 (0.004) C 0.268 (0.004) 0.100 (0.000) 0.271 (0.004) 0.271 (0.004) Nucleotide model, codon positions 1 B 0.408 (0.005) 0.313 (0.000) 0.362 (0.005) 0.362 (0.005) and 2 C 0.592 (0.005) 0.687 (0.000) 0.638 (0.005) 0.638 (0.005) Nucleotide model, codon position 3 B 0.923 (0.003) 0.998 (0.000) 0.912 (0.003) 0.994 (0.001) C 0.076 (0.003) 0.002 (0.000) 0.088 (0.003) 0.168 (0.004) Codon model, estimated frequency B 0.021 (0.001) 5 ϫ 10Ϫ11 (0.000) 0.016 (0.001) 0.016 (0.001) C 0.979 (0.001) 1.000 (0.000) 0.984 (0.001) 0.984 (0.001) Codon model, equal frequency B 0.362 (0.005) 0.011 (0.000) 0.349 (0.005) 0.349 (0.005) C 0.638 (0.005) 0.989 (0.000) 0.651 (0.005) 0.651 (0.005) Tree B has all gene copies diverging after the separation of bdelloid families as in Fig. 1B; in tree C the most divergent copies separate before the bdelloid radiation as in Fig.
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