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Dave Lunt @davelunt speakerdeck.com/davelunt slides available Georgios Koutsovoulos Mark Blaxter Sujai Kumar Comparative genomics of root knot nematodes: Tales of sex, hybridisation and adaptation Evolutionary Biology Group, University of Hull Institute of Evolutionary Biology, University of Edinburgh

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THE MELOIDOGYNE RKN SYSTEM Meloidogyne Reproduction • Mitotic parthenogens (apomixis) without chromosome pairs. Ancient asexuals? Asexuals- meiosis absent • Meiotic parthenogens (automixis) • Obligatory outbreeding sexuals with males & females (amphimixis) Sexuals- meiosis present Wide variety of reproductive modes in a single genus

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THE MELOIDOGYNE RKN SYSTEM Meloidogyne Reproduction Wide variety of reproductive modes in a single genus

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MELOIDOGYNE HYBRIDISATION Hybrid Speciation in Meloidogyne? Some previous work has suggested interspecific hybridisation may be involved with Meloidogyne asexual species Heliconius butterflies Lake Malawi cichlids Root knot nematodes?

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Is M. floridensis the parent of the asexuals? M. floridensis is found within the phylogenetic diversity of asexual species! It reproduces sexually by automixis! Could it be a parent of the asexual lineages via interspecific hybridisation? MELOIDOGYNE HYBRIDISATION GENOMICS M.floridensis M. ??? M. incognita M. javanica M. arenaria x apomicts parental species automict apomict apomict automict

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MELOIDOGYNE HYBRIDISATION GENOMICS Meloidogyne comparative genomics We have sequenced M. floridensis genome and compare to 2 other published Meloidogyne genomes M.floridensis M. ??? M. incognita M. javanica M. arenaria x apomicts parental species automict asexual, hybrid? sexual, parental? sexual, outgroup 100MB, 100x coverage, 15.3k protein coding loci

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Is M. floridensis the parent of the asexuals? 1. look at the within-genome patterns of diversity to determine hybrid nature of genomes! 2. look at phylogenetic relationships of all genes to study origins and parents MELOIDOGYNE HYBRIDISATION GENOMICS 1: Intra-genomic diversity 2: Phylogenomics Investigated using whole genome sequences and 2 distinct approaches;

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1. INTRA-GENOMIC ANALYSES Divergence of protein-coding alleles Lunt et al arXiv 2013 http://arxiv.org/abs/1306.6163 Coding sequences from each species were compared to loci in the same species! The percent identity of the best match was plotted Self identity comparisons Both M. incognita and M. floridensis show evidence of presence of many duplicates, while M. hapla does not

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1. INTRA-GENOMIC ANALYSES Divergence of protein-coding alleles Lunt et al arXiv 2013 http://arxiv.org/abs/1306.6163 Self identity comparisons Both M. incognita and M. floridensis show evidence of presence of many duplicates, while M. hapla does not This is exactly the pattern expected for hybrid genomes

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Is M. floridensis the parent of the asexuals? ! look at phylogenetic relationships of all genes to study origins and parents MELOIDOGYNE HYBRIDISATION GENOMICS 1: Intra-genomic diversity 2: Phylogenomics

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11 M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 Z M. incognita Z+Z 1 & 2 X+Y M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 Z M. incognita +Z X+Y M. hapla X Y M. floridensis X+Y C Scenario 4 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla D M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 Hybridisation hypotheses A B C D We have selected a broad range of possibilities informed by prior knowledge! We have tested their predictions phylogenetically

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M. hapla X M. floridensis X B Scenario M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 (A)! Whole genome duplication(s)

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13 M. hapla X M. floridensis X+Y C Scena M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. incognita Z (B)! M. incognita is an interspecific hybrid with M. floridensis as one parent

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M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y M. florid X+Y D Scenario X+Y (C)! M. incognita and M. floridensis are independent hybrids sharing one parent

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Z M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z X+Y (D)! M. floridensis is a hybrid and M. incognita is a secondary hybrid between M. floridensis and a 3rd parent

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2. PHYLOGENOMIC ANALYSES Testing by Phylogenomics Lunt et al arXiv 2013 http://arxiv.org/abs/1306.6163 M. hapla M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 A M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 B M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 X+Y C M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 X+Y D • Recover all genes from 3 genomes! • CDS orthologues determined by InParanoid! • 4018 ortholog clusters included all 3 species! • Retained those with a single copy in the outgroup M. hapla ! • ML Phylogenies of relationships between Mi and Mf gene copies! • Trees parsed and pooled to represent frequencies of different relationships

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17 Each tree contains a single M. hapla sequence as outgroup (black square) Grey square indicates relative frequency of those topologies Trees are pooled within squares into different patterns of relationships Grid squares represent different numbers of gene copies

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2. PHYLOGENOMIC ANALYSES Testing by Phylogenomics Lunt et al arXiv 2013 http://arxiv.org/abs/1306.6163 M. hapla M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 A M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 B M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 X+Y C M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 M. hapla X Z M. floridensis M. incognita X X+Z B Scenario 3 M. hapla X Z M. floridensis M. incognita X Z+Z A Scenario 1 & 2 X+Y D We assess the fit of the tree topologies to our hypotheses! • Five out of seven cluster sets, and 95% of all trees, support hybrid origins for both M. floridensis and M. incognita! • ie exclude hypotheses A and B! • Hypothesis C best explains 17 trees! • Hypothesis D best explains 1335 trees

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2. PHYLOGENOMIC ANALYSES Testing by Phylogenomics Lunt et al arXiv 2013 http://arxiv.org/abs/1306.6163 M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z M. hapla X Z M. floridensis M. incognita X X+Z M. hapla X Z M. floridensis M. incognita X Z+Z X+Y A M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z M. hapla X Z M. floridensis M. incognita X X+Z M. hapla X Z M. floridensis M. incognita X Z+Z X+Y B M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z M. hapla X Z M. floridensis M. incognita X X+Z M. hapla X Z M. floridensis M. incognita X Z+Z X+Y C M. floridensis is a parental species of “double hybrid” M. incognita with other parent unknown M. hapla X Y Z M. floridensis M. incognita X+Y Y+Z C Scenario 4 M. hapla X Y Z M. floridensis M. incognita X+Y (X+Y)+Z D Scenario 5 X Z M. floridensis M. incognita X X+Z B Scenario 3 X+Y Hypothesis D Conclusion:

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MELOIDOGYNE COMPARATIVE GENOMICS 1. Ongoing Work • Genomes in a phylogenetic design! • Testing effect of recombination & breeding system on genome change! • hybrids, inbred, outbred, loss of meiosis, TEs, mutational patterns, gene families Meloidogyne breeding system and genome evolution

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MELOIDOGYNE COMPARATIVE GENOMICS 2. Wild speculation Happy to discuss in the bar…! • ancient asexuality! • reproductive mode transitions! • adaptation through transgressive segregation! • the ‘hybrid threat’! • distinguishing single/multiple origins of apomicts! • contagious asexuality Dave Lunt Evolutionary Biology Group, University of Hull [email protected] davelunt.net speakerdeck.com/davelunt slides available

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Dave Lunt @davelunt speakerdeck.com/davelunt slides available Georgios Koutsovoulos Mark Blaxter Sujai Kumar Comparative genomics of root knot nematodes: Tales of sex, hybridisation and adaptation Evolutionary Biology Group, University of Hull Institute of Evolutionary Biology, University of Edinburgh [email protected] davelunt.net