Research: The objective of our research is to understand why nearly all animals and plants reproduce sexually, why the loss of sexual reproduction usually leads to early extinction. Very few species of animals and plants reproduce only asexually and those that do rarely comprise an entire genus, let alone a taxon of higher rank. Despite this and other evidence that most asexual species do not last long enough to evolve higher taxa, there is no agreed explanation of what causes their early extinction, or of why sexual reproduction is associated with evolutionary success. Our approach to this fundamental biological problem is to ask if there is any major exception - a higher-rank taxon that has evolved without sexual reproduction -- and, if so, to utilize it in studies to learn what has allowed it to escape extinction. The entire Class Bdelloidea of the Phylum Rotifera appears to be such an exception. Bdelloid rotifers are small fresh-water invertebrates comprising four families, 19 genera, and some 350 species. Males and meiosis are unknown. Instead, eggs are produced from oocytes by two mitotic divisions with no chromosome pairing and no reduction in chromosome number. Although remarkable, these observations do not preclude rare or unrecognized forms of sexual reproduction. We are therefor seeking more rigorous evidence that bdelloid rotifers have evolved asexually. Our principal approach makes use of the fact that the genome of a sexually-reproducing diploid contains two sets of chromosomes that are kept closely homologous by segregation of haplotypes and genetic drift. In contrast, if reproduction is only mitotic and if there is no genetic recombination, segregation cannot occur and the gradual accumulation of mutations will cause nucleotide sequences that initially are closely homologous to diverge, so that after millions of years individual genomes will no longer contain pairs of closely homologous chromosomes. In accordance with this expectation, we have found that in individual bdelloid rotifers the genome contains highly divergent copies of each gene we have examined (hsp82, RNApolIII, tbp, and tpi ). In contrast, as expected for sexually-reproducing diploids, we find only pairs of closely homologous copies in the genomes of individual rotifers of the other two classes within the phylum, the facultatively sexual Class Monogononta and the obligately sexual Class Seisonida. We are seeking definitive confirmation that bdelloids are not sexually-reproducing diploids (or polyploids) by employing fluorescent in situ hybridization to bdelloid chromosomes, a procedure that will directly reveal homologous chromosome pairs if they are present. While we are proceeding with this and with experiments to detect the possible occurrence in bdelloids of certain obscure and unprecedented forms of genetic exchange, we have also begun to examine bdelloid genomes for characteristics that may be associated with long-term asexuality. In this connection, we have made the remarkable observation that while retrotransposons are readily detected by polymerase chain reaction in the genomes of all other eukaryotes tested, including monogonont and seisonid rotifers, they are apparently absent in bdelloid rotifers. It would therefor appear that active retrotransposons cannot be retained in asexual lines over evolutionary time periods or that the absence of such elements is a pre-condition for the avoidance of extinction in asexual lines, a possibility that would ascribe to sexual reproduction a role in limiting the accumulation of insertion mutations. While screens for both RNA and DNA tranposons are continuing, we are also conducting computer searches of bdelloid DNA sequences to detect possible relict retrotranposons and, if found, to examine their phylogeny and characterize the nature of their defects. Opportunities for utilizing bdelloid rotifers in the study of basic genetic problems include investigations of genome structure, DNA repair, transposon control and proliferation,heterosis, and population genetic diversity.
Selected Publications: Gladyshev, E.A., M. Meselson and I.R. Arkhipova (2007). A deep-branching clade of retrovirus-like retrotransposons in bdelloid rotifers. Gene 390: 136-145. Gladyshev, E.A. and I.R. Arkhipova (2007). Telomere-associated endonuclease-deficient Penelope-like retroelements in diverse eukaryotes. Proc Natl Acad Sci U S A. 104: 9352-9357. Arkhipova, I.R. (2006). Distribution and phylogeny of Penelope-like elements in eukaryotes. Syst Biol. 55: 875-885. Arkhipova, I.R. and M. Meselson (2005). Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci U S A. 102: 11781-11786. Arkhipova, I. and M. Meselson (2005). Deleterious transposable elements and the extinction of asexuals. Bioessays 27: 76-85. Meselson, M. (2004). Explorations in the land of DNA and beyond. Nat Med. 10: 1034-1037. Pyatkov, K.I., I.R. Arkhipova, N.V. Malkova, D.J. Finnegan and M.B. Evgen'ev (2004). Reverse transcriptase and endonuclease activities encoded by Penelope-like retroelements. Proc Natl Acad Sci U S A 101: 14719-14724. Mark Welch D.B., M.P.Cummings, D.M Hillis and M. Meselson (2004). Divergent gene copies in the asexual class Bdelloidea (Rotifera) separated before the bdelloid radiation or within bdelloid families. Proc Natl Acad Sci U S A. 101: 1622-1625. Mark Welch J.L., D.B. Mark Welch and M.Meselson (2004). Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proc Natl Acad Sci U S A. 101: 1618-1621. Meselson M. (2003). Interview with Matthew Meselson. Bioessays 12: 1236-46. Mark Welch D.B. and M. Meselson (2003) Oocyte nuclear DNA content and GC proportion in rotifers of the anciently asexsual Class Bdelloidea. Biological Journal of the Linnean Society 79: 85-91. Arkhipova, I.R., K.I. Pyatkov, M. Meselson and M.B. Evgen'ev (2003). Retroelements containing introns in diverse invertebrate taxa. Nature Genetics 33:123-124. Arkhipova, I. and H. G. Morrison (2001). Three retrotransposon families in the genome of Giardia lamblia: Two telomeric, one dead. Proc. Natl. Acad. Sci (USA) 98: 14497-14502. Mark Welch, D. (2001). Early contributions of molecular phylogenetics to understanding the evolution of Rotifera. Hydrobiologia 446/447: 315-322. Mark Welch, D. and M. Meselson. (2001). Rates of nucleotide substitution in sexual and anciently asexual rotifers. Proc. Natl. Acad. Sci (USA) 98: 6720-6724. Mark Welch, D. and M. Meselson.(2001). A survey of introns in three genes of rotifers. Hydrobiologia 446/447: 333-336. Mark Welch, D. (2000). Evidence from a protein-coding gene that acanthocephalans are rotifers. Invertebrate Biology 119: 17-26. Arkhipova, I. and M. Meselson. (2000). Transposable elements in sexual and ancient asexual taxa. Proc. Natl. Acad. Sci. (USA) 97: 14473-14477. Mark Welch, D. and M. Meselson. (2000). Evidence for the evolution of bdelloid rotifers without sexual recombination or genetic exchange. Science 288: 1211-1215. Mark Welch, J. and M. Meselson. (1998). Karyotypes of bdelloid rotifers from three families. Hydrobiologia 387/388: 403 - 407. Mark Welch, D. and M. Meselson. (1998). Measurements of the genome size of the monogonont rotifer Brachionus plicatilis and of the bdelloid rotifers Philodina roseola and Habrotrocha constricta. Hydrobiologia 387/388: 395-402.
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