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

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Presentation on theme: "DEPARTMENT OF BIOLOGY using self-fertile nematodes to explore the evolution of genes, genomes, and reproductive isolation Eric Haag."— Presentation transcript:

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

2 Caenorhabditis reproductive diversity in free-living nematodes (Class Chromadorea) Denver et al Oschieus Panagrolaimus Pristionchus D dioecious/gonochoristic H selfing hermaphroditic P parthenogenic

3 Caenorhabditis remanei: XX females, XO males Cristel Thomas

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

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

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

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

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

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

10 C. briggsae shares core sex pathway… fem genes perform conserved male-promoting roles in the soma Hill et al (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. elegans lineage—no C. briggsae ortholog Clifford et al. 2001, Nayak et al (Schedl Lab) C. briggsae XX sperm also requires species-specific F-box protein, she-1 Guo et al (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 (Ellis Lab) Cbr-fem-3(nm63) XX (virgin)

12 …but regulates XX spermatogenesis differently. fog-2 a recent duplication in C. elegans lineage—no C. briggsae ortholog Clifford et al. 2001, Nayak et al (Schedl Lab) C. briggsae XX sperm also requires species-specific F-box protein, she-1 Guo et al (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 (Ellis Lab) Cbr-fem-3(nm63) XX (virgin)

13 …but regulates XX spermatogenesis differently. fog-2 a recent duplication in C. elegans lineage—no C. briggsae ortholog Clifford et al. 2001, Nayak et al (Schedl Lab) C. briggsae XX sperm also requires species-specific F-box protein, she-1 Guo et al (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 (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 (Haag & Wickens labs) germline phenotypic evolution targets translational controls conserved & species-specific genes both important context changes roles of homologous genes Cbr-gld-1(nm68) Ce-gld-1(q485) sperm fate oocyte fate Beadell et al. PNAS (2011)

15 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? 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

16 mutational load and impact on genome projects Ilya Ruvinsky, 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) other consequences we have noticed & explored

17 impact on genome projects Ilya Ruvinsky, 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) consequences we have noticed & explored

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

21 impact on genome projects Ilya Ruvinsky, 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) consequences we have noticed & explored

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

23 Lower proportion of strongly female- biased transcribed Strongly male-biased transcripts less male-specific but, in C. elegans & C. briggsae: Strong male bias more common than strong female bias in all species comparing the comparisons 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  2 test, compared to genes detected in C. remanei * p < 0.05 ** p < 0.01 *** p < Thomas et al. 2012

26 impact on genome projects Ilya Ruvinsky, 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) consequences we have noticed & explored

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” selfing parents. 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.” Caenorhabditis is 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 Caenorhabditis Oschieus Panagrolaimus Pristionchus Selfing: a deal with the Devil?

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-NIGMSHHMI (undergrad fellowships)


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