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[
International Worm Meeting,
2015]
Two partially-interfertile pairs of Caenorhabditis species permit genetic and developmental dissection of the intrinsic barriers to reproduction that maintain species boundaries. Interspecies F1 hybrids of C. briggsae and C. nigoni suffer high embryonic inviability, especially in males, but virtually no mortality occurs from L2 onward in development. This pattern begs further consideration of the evolution of development in the speciation process. The production of F1 hybrid males is especially poor at cold temperatures, indicating genotype-environment interactions in the manifestation of Haldane's rule. Moreover, a fertilization advantage of C. briggsae sperm bearing the X-chromosome exacerbates the rarity of males in interspecies crosses, demonstrating the first evidence for a role of gametic selection in the severity of Haldane's rule. Controlled crosses rule out mito-nuclear incompatibility as a source of the extensive cross-direction asymmetry in hybrid dysfunction (F1 hybrids are worse from C. briggsae mothers), despite high molecular divergence of their mitochondrial genomes. Complementary experiments with C. remanei and C. latens similarly rule out an important role for mito-nuclear hybrid incompatibilities. Instead, genetic incompatibilities between the X chromosome and autosomal loci are a likely source of reproductive isolation. .
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[
International Worm Meeting,
2009]
Operons are curiously pervasive in the C. elegans genome, containing roughly 15% of its encoded genes, more than 95% of which have been preserved in the C. briggsae genome over the course of evolution. However, determination of the common forces that promote the origin and/or maintenance of these genic structures has proved elusive. Here we demonstrate that nearly all operon-encoded genes are expressed in germline tissue, based on microarray and large-scale in situ hybridization data. Genes expressed during spermatogenesis, however, are almost completely excluded from operons. We also find that operons cluster non-randomly along chromosomes and that monocistronic genes that are expressed in the germline aggregate near operons. Nevertheless, the molecular functions of operon-encoded genes largely are independent of germline expression. Thus, gene expression in germline tissue is likely to have played an integral role in the evolution of C. elegans'' operons, and consequently in the evolution of genome organization in this and related species.
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[
International Worm Meeting,
2011]
The recent discovery that the new species C. sp. 9 could hybridize with C. briggsae to generate viable and fertile F1 female progeny opens the door, for the first time, to applying the power of the Caenorhabditis model system to what Darwin called the "mystery of mysteries": speciation (Woodruff et al. 2010). We have begun exploiting this system to investigate the evolution and genetics of reproductive isolation between these species in several dimensions: pre-mating isolation, post-mating pre-zygotic isolation, and post-zygotic isolation. At the pre-mating level, we are using chemotaxis assays to determine the extent of species-specificity in attraction to female mating pheromone produced by C. sp. 9. While we find that male attraction appears to attenuate as a function of evolutionary divergence across the phylogeny, this "love potion no. 9" may not provide a species-specific mating signal. Post-zygotically, we confirm that inter-species crosses conform to Haldane's rule in that males are disproportionately detrimentally affected in hybrids and that parent-of-origin asymmetries are rampant, in accord with Darwin's corollary to Haldane's rule (Woodruff et al. 2010). In addition, we document significant within-species heritable variation for between-species hybrid incompatibility. This phenomenon of "variable reproductive isolation" is emerging as a general pattern in many organisms, and C. briggsae provides an exceptional system to dissect its genetic causes. We are now applying QTL mapping approaches with recombinant inbred lines (RILs) to determine the genetic basis to this intra-specific variation in hybrid incompatibility. I will also discuss a potentially new incipient speciation system involving C. remanei and strains from China.
Woodruff GC, Eke O, Baird SE, Felix MA, Haag ES (2010). Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186: 997-1012.
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Evolutionary Biology of Caenorhabditis and Other Nematodes,
2014]
Determining the causes and evolution of reproductive barriers to gene flow between populations, speciation, is the key to understanding the origin of diversity in nature. Many species manifest hybrid breakdown when they intercross, characterized by increasingly exacerbated problems in later generations of hybrids. Recently, Caenorhabditis nematodes have emerged as a genetic model for studying speciation, and here we investigate the nature and causes of hybrid breakdown between C. remanei and C. latens (formerly C. sp. 23). We quantify partial F1 hybrid inviability and extensive F2 hybrid inviability; the ~75% F2 embryonic arrest occurs primarily during gastrulation or embryonic elongation. Moreover, F1 hybrid males exhibit Haldane's rule asymmetrically for both sterility and inviability, being strongest when C. remanei serves as maternal parent. We show that the mechanism by which sterile hybrid males are incapable of transferring sperm or a copulatory plug involves defective gonad morphogenesis, which we hypothesize results from linker cell defects in migration and/or cell death during development. I will also discuss these findings in light of inter-species hybrids between C. briggsae and C. nigoni (formerly C. sp. 9), ongoing investigations into the evolution of reproductive isolation in Caenorhabditis, and conceptual implications. This first documented case of partial hybrid male sterility in Caenorhabditis follows expectations of Darwin's corollary to Haldane's rule for asymmetric male fitness, providing a powerful foundation for molecular dissection of intrinsic reproductive barriers and divergence of genetic pathways controlling organ morphogenesis.
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[
International Worm Meeting,
2003]
The availability of diverse and comprehensive sets of genomic data for C. elegans and C. briggsae allows opportunities to investigate biological issues that were unforeseen in the initial stages of data aquisition. In this study, we apply quantitative methods from molecular evolutionary population genetics to a genomic comparison between C. elegans and C. briggsae in the context of phenotypes identified by RNAi (Kamath et al. 2003). We calculated and partitioned the rates of molecular evolution of nearly 10,000 coding regions throughout the C. elegans genome among the multiple phenotypic classes that were identified from published RNAi data. We find that loci with scoreable RNAi phenotypes evolve slowly and have strongly biased codon usage. We also find that the degree of sterility conferred by RNAi correlates negatively with rates of protein evolution and that loci involved in sterility tend to evolve slower than loci that adversely influence embryonic survival. These findings bear on general issues related to our understanding of how the forces that influence molecular evolution (e.g. mutation, selection, recombination) relate to phenotypes and phenotypic evolution. R. S. Kamath et al. 2003. Nature. 421: 231-237.
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[
Development & Evolution Meeting,
2008]
A perennial difficulty in understanding the evolutionary past of C. elegans and its relatives is how long ago different species shared common ancestors and how long ago a predominantly self-fertilizing mode of reproduction evolved. The answers to these questions have important implications for interpreting present-day observations on phenotypes and phenotypic variation, genomic patterning, and molecular genetic and developmental pathways. To address these issues of lineage and breeding system age, I have assessed patterns of divergence using "partial genomes" of six species of Caenorhabditis derived from expressed sequence tag (EST) datasets. By applying explicit molecular evolutionary models to these data, I infer dates of common ancestry between C. elegans and its closest relatives. Furthermore, relaxation of purifying selection following the onset of a primarily selfing mode of reproduction, as quantified with patterns of amino acid substution and the decay of biased codon usage, suggests that selfing likely evolved in the not-too-distant past.
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[
International Worm Meeting,
2003]
Sperm limited fecundity in selfing C. elegans hermaphrodites has been explained to be the consequence of a trade-off between selection for greater total fecundity and more rapid turnover of generations. Greater numbers of sperm increase the total number of progeny produced by a hermaphrodite, but delay the onset of fertilization and therefore reduce the intrinsic rate of population growth. Both empirical and theoretical work support this general explanation (Hodgkin & Barnes 1991; Barker 1992). However, the question remains: can this simple model explain the actual numbers of sperm produced by C. elegans hermaphrodites? In this study, I extend a well-known population model to calculate the expected number of sperm that hermaphrodites would produce to maximize fitness (i.e. the intrinsic rate of growth). I apply literature-based and new empirical estimates of rates of gamete production and the fraction of sperm produced during larval development to the model. I find that the model predicts sperm counts consistent with observed sperm numbers in C. elegans hermaphrodites, given available empirical data, and provided that precocious larval production of sperm is taken into account. Several testable hypotheses follow from the model regarding how natural selection and environmental variation may influence sperm production among populations or among species with a similar mode of reproduction. J. Hodgkin & T.M. Barnes. 1991. Proc. R. Soc. London B. 246: 19-24; D.M. Barker. 1992. Evolution. 46: 1951-1955.
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[
West Coast Worm Meeting,
2002]
C. elegans natural populations are comprised of self-fertilizing hermaphrodites and an unknown, but presumably small, percentage of males. Males arise as a consequence of rare X-chromosome non-disjunction events during meiosis in hermaphrodites or via outcrossing with males (Hodgkin, Horvitz, and Brenner 1979). Laboratory studies have identified variation among wild-caught strains in X-chromosome non-disjunction rates and male reproductive success (Hodgkin and Doniach 1997). However, like much of C. elegans ecology and natural history, the incidence of males and of outcrossing in natural populations remains unknown. We are working to address the question of sex ratio in natural populations by developing a molecular approach to assay male frequency. Our method utilizes semi-quantitative rtPCR to describe the abundance of a male-specific mRNA transcript relative to a control transcript that is expressed in both sexes. We are currently (1) constructing a standard curve of relative expression levels from lab samples of known sex ratio, from which we will be able to infer the frequency of males in unknown laboratory or natural samples, and (2) ascertaining the species specificity of the primers that we are employing in this method.
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[
West Coast Worm Meeting,
2002]
Natural selection can produce a correlation between local recombination rates and levels of neutral DNA polymorphism as a consequence of genetic hitchhiking and background selection. Theory suggests that selection at linked sites should affect patterns of neutral variation in partially selfing populations more dramatically than in outcrossing populations. However, empirical investigations of selection at linked sites have focused primarily on outcrossing species. To assess the potential role of selection as a determinant of neutral polymorphism in the context of partial self-fertilization, we conducted a multivariate analysis of single nucleotide polymorphism (SNP) density throughout the genome of the nematode Caenorhabditis elegans. We based the analysis on a published SNP data set (Wicks et al. 2001) and used a sliding-window approach to calculate SNP densities, recombination rates, and gene densities across all six chromosomes. Our analyses identify a strong, positive correlation between recombination rate and neutral polymorphism (as estimated by SNP density) across the genome of C. elegans. Furthermore, we find that levels of neutral polymorphism are lower in gene-dense regions than in gene-poor regions. Our results suggest that a neutral explanation alone cannot sufficiently explain the observed patterns. Consequently, we interpret these findings as evidence that natural selection shapes genome-wide patterns of neutral polymorphism in C. elegans. Our study provides the first demonstration of such an effect in a partially selfing animal. Explicit models of genetic hitchhiking and background selection can each adequately describe the relationship between recombination rate and SNP density, but only when they incorporate selfing rate. Non-linear regression fitting of genetic hitchhiking and background selection models to these data allow the estimation of parameters used in the models, such as outcrossing rate, genomic deleterious mutation rate, and average selection coefficient against deleterious mutations.
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[
International C. elegans Meeting,
2001]
Genes that are involved in reproduction or that have sex-limited expression clearly interest evolutionists due to their potential role in fitness. Theory suggests that such gene classes may also represent prime candidates for rapid evolution by sexual selection, and that loci involved in processes of rapid antagonistic coevolution should accumulate non-randomly on chromosomes. We apply a functional genomics perspective to the evolutionary issue of gene spatial arrangement using data comprising >90% of the genes predicted to be present in the Caenorhabditis elegans genome. This study demonstrates an approach by which microarray technology may be used to distinguish classes of genes for use in the genomic-scale testing of predictions generated by evolutionary theory-and illustrates some limitations of current genomic evolutionary theory. Randomization tests that take into account the physical positions of loci show that germline-related genes are distributed in an aggregated fashion along chromosomes. Furthermore, our findings indicate that germline-related and gender-related loci are represented disproportionately in regions of low recombination and that germline-related and gender-related loci are underrepresented on the X chromosome. Although definitive conclusions regarding the causes of these genomic patterns are premature, we hypothesize that processes ranging from mating system byproducts to biochemical constraints during meiosis and stabilizing selection may account for different components of our observations.