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DEPARTMENT OF BIOLOGY

u sing self-fertile nematodes to explore the evolution of genes, genomes, and reproductive isolation Eric Haag. DEPARTMENT OF BIOLOGY. reproductive diversity in free-living nematodes (Class Chromadorea ). Oschieus. Caenorhabditis. D dioecious / gonochoristic H selfing hermaphroditic

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DEPARTMENT OF BIOLOGY

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  1. using self-fertile nematodes to explore the evolution of genes, genomes, and reproductive isolation Eric Haag DEPARTMENT OF BIOLOGY

  2. reproductive diversity in free-living nematodes (Class Chromadorea) Oschieus Caenorhabditis Ddioecious/gonochoristic Hselfing hermaphroditic Pparthenogenic Pristionchus Panagrolaimus Denver et al. 2011

  3. Caenorhabditis remanei: XX females, XO males Cristel Thomas

  4. gonad C. briggsaeXX young adult self-fertile hermaphrodites: limited spermatogenesis in XX female soma

  5. repeated evolution of selfing in Caenorhabditis briggsae japonica C. sp.10 brenneri C. sp.11 remanei C. sp.16 elegans C. sp. 5 C. sp. 9 transition to selfing gonochoristic ancestor

  6. a model system for understanding convergent evolution C. briggsae C. japonica C. brenneri C. remanei C. elegans C. sp.10 C. sp.16 C. sp.11 C. sp. 5 C. sp. 9 • How many different ways are there to produce a hermaphrodite? • Once a lineage becomes selfing, are there reproducible consequences? gonochoristic ancestor C. briggsae

  7. genetic sex determination in C. elegans How do XX hermaphrodites make sperm?

  8. How C. elegansdoes it: translational repressors regulate germ line sex determination required for XX sperm gld-1 fog-2 XO XX fem-1 fem-2 fem-3 tra-2 tra-3 sperm her-1 tra-1 fbf-1/2 nos-3 limit XX sperm Kimble, Schedl Labs

  9. C. briggsaeshares core sex pathway… • tra-1/2/3 perform conserved female-promoting roles • Kuwabara1996, de Bono & Hodgkin 1996, Kelleher et al. 2008 (Haag and Pilgrim labs) Cbr-tra-2 Cbr-tra-2 Kelleher et al. 2008

  10. C. briggsaeshares core sex pathway… • fem genes perform conserved male-promoting roles in the soma • Hill et al. 2006 (Haag and Pilgrim labs) • sperm-promoting targets of TRA-1 (fog-1 & fog-3) also conserved • Chen & Ellis 2001, Cho et al., 2004 (Ellis lab) Cbr-fem-3(nm63) XO tail

  11. …but regulates XX spermatogenesis differently. • fog-2 a recent duplication in C. eleganslineage—no C. briggsaeortholog • Clifford et al. 2001, Nayak et al. 2005 (Schedl Lab) • C. briggsaeXX sperm also requires species-specific F-box protein, she-1 • Guo et al. 2009 (Ellis Lab) • C. briggsae fem genes not necessary for XX spermatogenesis • Hill et al., 2006 (Haag Lab) • XX & XO spermatogenesis depends on Tip60 histone acetyl transferase activity • Guo et al. 2013 (Ellis Lab) Cbr-fem-3(nm63) XX (virgin)

  12. …but regulates XX spermatogenesis differently. • fog-2 a recent duplication in C. eleganslineage—no C. briggsaeortholog • Clifford et al. 2001, Nayak et al. 2005 (Schedl Lab) • C. briggsaeXX sperm also requires species-specific F-box protein, she-1 • Guo et al. 2009 (Ellis Lab) • C. briggsae fem genes not necessary for XX spermatogenesis • Hill et al., 2006 (Haag Lab) • XX & XO spermatogenesis depends on Tip60 histone acetyl transferase activity • Guo et al. 2013 (Ellis Lab) Cbr-fem-3(nm63) XX (virgin)

  13. …but regulates XX spermatogenesis differently. • fog-2 a recent duplication in C. eleganslineage—no C. briggsaeortholog • Clifford et al. 2001, Nayak et al. 2005 (Schedl Lab) • C. briggsaeXX sperm also requires species-specific F-box protein, she-1 • Guo et al. 2009 (Ellis Lab) • C. briggsae fem genes not necessary for XX spermatogenesis • Hill et al., 2006 (Haag & Pilgrim Labs) • XX & XO spermatogenesis depends on Tip60 histone acetyl transferase activity • Guo et al. 2013 (Ellis Lab) Cbr-fem-3(nm63) XX (virgin)

  14. …but regulates XX spermatogenesis differently. • homologs play opposite roles, but have similar biochemical activities. • Beadell et al., 2011 (Haag Lab), Liu et al. 2012 (Haag & Wickens labs) sperm fate oocyte fate Cbr-gld-1(nm68) Ce-gld-1(q485) Beadellet al. PNAS (2011) • germline phenotypic evolution targets translational controls • conserved & species-specific genes both important • context changes roles of homologous genes

  15. expected consequences of sexual mode • facultative selfing • replication of high-fitness genotypes • reproductive assurance upon colonization • maximal population growth (few males) • genomes naturally homozygous—recessive deleterious alleles purged • obligate outcrossing • faster adaptation to new environments and pathogens • recombination allows precise selection for/against new mutations • must colonize in groups • males reduce population growth • genomes highly polymorphic—inbreed before sequencing?

  16. other consequences we have noticed & explored • mutational load and impact on genome projects • IlyaRuvinsky, U. of Chicago • reduced genome & transcriptome size • Barbara Meyer (Berkeley) Erich Schwarz (CalTech/Cornell) Brian Oliver (NIH) • evolution of sex-biased gene expression • Brian Oliver (NIH) • “selfing syndrome” and reproductive isolation • Asher Cutter (Univ. of Toronto)

  17. consequences we have noticed & explored • impact on genome projects • IlyaRuvinsky, U. of Chicago • reduced genome & transcriptome size • Barbara Meyer (Berkeley) Erich Schwarz (CalTech/Cornell) Brian Oliver (NIH) • evolution of sex-biased gene expression • Brian Oliver (NIH) • relaxed sexual conflict and reproductive isolation • Asher Cutter (Univ. of Toronto)

  18. apparent genome shrinkage in hermaphroditic species Computational elimination of alternative alleles still leaves “extra” DNA and genes. Is this real?

  19. transcriptome size also correlates with sexual mode Thomas et al. 2012

  20. likely mechanism of genome shrinkage: indel segregation distortion in males X A XX progeny (smaller autosome) XO progeny (larger autosome) Wang et al. 2010, Keller Lab

  21. consequences we have noticed & explored • impact on genome projects • IlyaRuvinsky, U. of Chicago • reduced genome & transcriptome size • Barbara Meyer (Berkeley) Erich Schwarz (CalTech/Cornell) Brian Oliver (NIH) • evolution of sex-biased gene expression • Brian Oliver (NIH) • relaxed sexual conflict and reproductive isolation • Asher Cutter (Univ. of Toronto)

  22. comparing expression between XX and XO sexes Significant sex-bias Significant sex-bias over 10-fold Thomas et al. 2012

  23. comparing the comparisons • Strong male bias more common than strong female bias in all species but, in C. elegans& C. briggsae: • Lower proportion of strongly female-biased transcribed • Strongly male-biased transcripts less male-specific Thomas et al. 2012

  24. relaxed sexual regulation of “male genes” >10X male-biased Thomas et al. 2012

  25. highly sex-biased C. remanei genes disproportionately absent from hermaphrodite genomes 2test, compared to genes detected in C. remanei * p < 0.05 ** p < 0.01 *** p < 0.001 Thomas et al. 2012

  26. consequences we have noticed & explored • impact on genome projects • IlyaRuvinsky, U. of Chicago • reduced genome & transcriptome size • Barbara Meyer (Berkeley) Erich Schwarz (CalTech/Cornell) Brian Oliver (NIH) • evolution of sex-biased gene expression • Brian Oliver (NIH) • parallel loss of seminal peptides—orphan signaling molecules? • Josh Singer (UMD) • sexual conflict and reproductive isolation • Asher Cutter (Univ. of Toronto)

  27. Weak Inbreeder/Strong Outcrosser (WISO) • Hypothesis (Brandvain and Haig, 2005) • “In crosses between plants with differing mating systems, outcrossing parents are expected to “overpower” selfingparents. Prezygotically, such overpowering explains a common pattern of incompatibility, in which pollen from self-incompatible populations fertilizes ovules of self-compatible individuals but the reciprocal cross fails. Such conflicts may strengthen reproductive barriers between populations, contributing to speciation.” • Caenorhabditisis one of the few animal systems where WISO might also operate? • Ongoing collaboration with Asher Cutter lab suggests it does.

  28. Speculations on sexual mode and macroevolution: • Relaxed sexual selection in selfers may accelerate and/or reinforce reproductive isolation of newly selfing taxa. • Genome shrinkage rapidly eliminates genes required to revert to robust outcrossing. • Selfing species vulnerable to infrequent catastrophes, leading to group selection against selfing over long evolutionary time scales.

  29. Selfing: a deal with the Devil? Oschieus Caenorhabditis Pristionchus Panagrolaimus

  30. thanks! • Alana Beadell • Qinwen Liu • Cristel Thomas • Gavin Woodruff • Becca Matteson • Da Yin • Cutter Lab (Univ. of Toronto) • Meyer Lab (Berkeley) • Oliver Lab (NIH) • Pilgrim Lab (Univ. of Alberta) • Ruvinsky Lab (U Chicago) • Harold Smith (NIH) • Erich Schwarz (Cornell) • Wickens Lab (Univ. of Wisconsin) NSF-IOSNIH-NIGMS HHMI(undergrad fellowships)

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