Signatures of the Evolution of Parthenogenesis and Cryptobiosis in the Genomes of Panagrolaimid Nematodes

Schiffer, Philipp H.; Danchin, Etienne G. J.; Burnell, Ann M.; Creevey, Christopher J.; Wong, Simon; Dix, Ilona; O’Mahony, Georgina; Culleton, Bridget A.; Rancurel, Corinne; Stier, Gary; Martínez-Salazar, Elizabeth A.; Marconi, Aleksandra; Trivedi, Urmi; Kroiher, Michael; Thorne, Michael A. S.; Schierenberg, Einhard; Wiehe, Thomas; Blaxter, Mark

doi:10.1016/j.isci.2019.10.039

Cited by 34 publications

(77 citation statements)

References 125 publications

(157 reference statements)

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“…[75, 76] and some Panagrolaimus spp. [77]). Polyspermy in worms is thought to be rare, with a single description in the rodent filarial worm Acanthocheilonema viteae [78]; more is understood in regard to the mechanisms by which polyspermy is prevented [79-81].…”

Section: Discussionmentioning

confidence: 99%

A genome resequencing-based genetic map reveals the recombination landscape of an outbred parasitic nematode in the presence of polyploidy and polyandry

Doyle

Laing

Bartley

et al. 2017

Preprint

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The parasitic nematode Haemonchus contortus is an economically and clinically important pathogen of small ruminants, and a model system for understanding the mechanisms and evolution of traits such as anthelmintic resistance. Anthelmintic resistance is widespread and is a major threat to the sustainability of livestock agriculture globally; however, little is known about the genome architecture and parameters such as recombination that will ultimately influence the rate at which resistance may evolve and spread. Here we performed a genetic cross between two divergent strains of H. contortus, and subsequently used whole-genome re-sequencing of a female worm and her brood to identify the distribution of genome-wide variation that characterises these strains. Using a novel bioinformatic approach to identify variants that segregate as expected in a pseudo-testcross, we characterised linkage groups and estimated genetic distances between markers to generate a chromosome-scale F1 genetic map composed of 1,618 SNPs. We exploited this map to reveal the recombination landscape, the first for any parasitic helminth species, demonstrating extensive variation in recombination rate within and between chromosomes. Analyses of these data also revealed the extent of polyandry, whereby at least eight males were found to have contributed to the genetic variation of the progeny analysed. Triploid offspring were also identified, which we hypothesise are the result of nondisjunction during female meiosis or polyspermy. These results expand our knowledge of the genetics of parasitic helminths and the unusual life-history of H. contortus, and will enable more precise characterisation of the evolution and inheritance of genetic traits such as anthelmintic resistance. This study also demonstrates the feasibility of whole-genome resequencing data to directly construct a genetic map in a single generation cross from a non-inbred non-model organism with a complex lifecycle.Author summaryRecombination is a key genetic process, responsible for the generation of novel genotypes and subsequent phenotypic variation as a result of crossing over between homologous chromosomes. Populations of strongylid nematodes, such as the gastrointestinal parasites that infect livestock and humans, are genetically very diverse, but little is known about patterns of recombination across the genome and how this may contribute to the genetics and evolution of these pathogens. In this study, we performed a genetic cross to quantify recombination in the barber’s pole worm, Haemonchus contortus, an important parasite of sheep and goats. The reproductive traits of this worm make standard genetic crosses challenging, but by generating whole-genome sequence data from a female worm and her offspring, we identified genetic variants that act as though they come from a single mating cross, allowing the use of standard statistical approaches to build a genetic map and explore the distribution and rates of recombination throughout the genome. A number of genetic signatures associated with H. contortus life history traits were revealed in this analysis: we extend our understanding of multiple paternity (polyandry) in this species, and provide evidence and explanation for sporadic increases in chromosome complements (polyploidy) among the progeny. The resulting genetic map will aid in population genomic studies in general and enhance ongoing efforts to understand the genetic basis of resistance to the drugs used to control these worms, as well as for related species that infect humans throughout the world.

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Section: Discussionmentioning

confidence: 99%

A genome resequencing-based genetic map reveals the recombination landscape of an outbred parasitic nematode in the presence of polyploidy and polyandry

Doyle

Laing

Bartley

et al. 2017

Preprint

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“…Nevertheless, the nematode Panagrolaimus davidi is characterized by both meiotic asexuality and triploidy [33] (see Supplementary Table 1 for details).…”

Section: Overview Of Species and Genomes Studiedmentioning

confidence: 99%

“…In more recent asexuals, reported levels of HGT appear mostly low, e.g. in Panagrolaimus (0.63% -0.66%) and in two tardigrade species (0.8% -0.97%) [19,33,39]. The only genome with a high reported fraction of HGT (2.8%) outside of the rotifers is the springtail F. candida [26].…”

Section: Horizontal Gene Transfermentioning

confidence: 99%

Genomic features of parthenogenetic animals

Jaroň

Bast²,

Nowell

et al. 2018

Preprint

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Evolution under asexuality is predicted to impact genomes in numerous ways, but empirical evidence remains unclear. Case studies of individual asexual animals have reported peculiar genomic features which were suggested to be caused by asexuality, including high heterozygosity, a high abundance of horizontally acquired genes, a low transposable element load, or the presence of palindromes. We systematically characterized these genomic features in published genomes of 26 asexual animals representing at least 18 independent transitions to asexuality. Surprisingly, not a single feature is systematically replicated across a majority of these transitions, suggesting that no genomic feature is characteristic of asexuality and that previously reported patterns were lineage specific rather than caused by asexuality. We found that only asexuals of hybrid origin were characterized by high heterozygosity levels. Asexuals that were not of hybrid origin appeared to be largely homozygous, independently of the cellular mechanism underlying asexuality. Overall, despite the importance of recombination rate variation for the evolution of sexual animal genomes, the genome-wide absence of recombination does not appear to have had the dramatic effects which are expected from classical theoretical models. The reasons for this are probably a combination of lineage-specific patterns, impact of the origin of asexuality, and a survivorship bias of asexual lineages. Box 1: Transitions to asexualityMeiotic sex and recombination evolved once in the common ancestor of eukaryotes [41].Asexual animals therefore derive from a sexual ancestor, but how transitions from sexual to asexual reproduction occur can vary and have different expected consequences for the genome [13]. Hybrid origin:Hybridization between sexual species can generate hybrid females that reproduce asexually [13,42]. Asexuality caused by hybridization can generate a highly heterozygous genome, depending on the divergence between the parental sexual species prior to hybridization. Hybridization can also result in a burst of transposable element activity [12]. Intraspecific origins: Endosymbiont infection. Infection with intracellular endosymbionts (such asWolbachia, Cardinium or Rickettsia) can cause asexuality, a pattern that is frequent in species with haplodiploid sex determination [43]. This type of transition often (but not always) results in fully homozygous lineages because induction of asexuality frequently occurs via gamete duplication (see Box 2). Spontaneous mutations/Contagious asexuality. Spontaneous mutations can alsounderlie transitions from sexual to asexual reproduction. In addition, asexual females of some species produce males that mate with females of sexual lineages, and thereby generate new asexual strains (contagious asexuality). In both cases, the genomes of incipient asexual lineages are expected to be very similar to those of their sexual relatives and subsequent changes should be largely driven by the cellular mechanism underlying asexuality (Box 2). an...

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“…This AI method was used again to assess the total contribution of genes of non-metazoan origin in the whole genome of the bdelloid rotifer once it was sequenced [ 18 ]. Using custom Perl scripts, our laboratory and collaborators also used AI to identify candidate HGT of non-metazoan origin in the genome of the plant-parasitic nematode Globodera rostochiensis [ 19 ], in the genomes of several panagrolaimid nematodes [ 20 ] as well as in the transcriptomes of the nematodes Nacobbus aberrans [ 21 ], Xiphinema index [ 22 ] and other as yet unpublished genomes. Calculation of AI scores for whole proteomes had previously been implemented in a software called AlienG [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life

Rancurel

Legrand

Danchin

2017

Genes

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Horizontal gene transfer (HGT) is the transmission of genes between organisms by other means than parental to offspring inheritance. While it is prevalent in prokaryotes, HGT is less frequent in eukaryotes and particularly in Metazoa. Here, we propose Alienness, a taxonomy-aware web application available at . Alienness parses BLAST results against public libraries to rapidly identify candidate HGT in any genome of interest. Alienness takes as input the result of a BLAST of a whole proteome of interest against any National Center for Biotechnology Information (NCBI) protein library. The user defines recipient (e.g., Metazoa) and donor (e.g., bacteria, fungi) branches of interest in the NCBI taxonomy. Based on the best BLAST E-values of candidate donor and recipient taxa, Alienness calculates an Alien Index (AI) for each query protein. An AI > 0 indicates a better hit to candidate donor than recipient taxa and a possible HGT. Higher AI represent higher gap of E-values between candidate donor and recipient and a more likely HGT. We confirmed the accuracy of Alienness on phylogenetically confirmed HGT of non-metazoan origin in plant-parasitic nematodes. Alienness scans whole proteomes to rapidly identify possible HGT in any species of interest and thus fosters exploration of HGT more easily and largely across the tree of life.

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Signatures of the Evolution of Parthenogenesis and Cryptobiosis in the Genomes of Panagrolaimid Nematodes

Cited by 34 publications

References 125 publications

A genome resequencing-based genetic map reveals the recombination landscape of an outbred parasitic nematode in the presence of polyploidy and polyandry

A genome resequencing-based genetic map reveals the recombination landscape of an outbred parasitic nematode in the presence of polyploidy and polyandry

Genomic features of parthenogenetic animals

Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life

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