While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, there are a small number of organisms that are testament to the contrary. The root-knot nematodes Meloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic parthenogenesis but have a broader host range, a wider geographical distribution, and a greater agricultural impact than their sexual relatives (Fig 1) [1]. Remarkably, some of these species even have the ability to overcome host resistance [2], suggesting a mechanism for adaptation in the absence of sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fully understood. Previous genome sequencing of Meloidogyne has shown that the genome of one of these species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid), with a further study suggesting that M. incognita may be the result of multiple additive hybridisation events: a hybrid of a hybrid [4]

Eves-van den Akker, Sebastian

Jones, John T

PLoS Genetics

English

While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, there are a small number of organisms that are testament to the contrary. The root-knot nematodes Meloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic parthenogenesis but have a broader host range, a wider geographical distribution, and a greater agricultural impact than their sexual relatives (Fig 1). Remarkably, some of these species even have the ability to overcome host resistance, suggesting a mechanism for adaptation in the absence of sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fully understood. Previous genome sequencing of Meloidogyne has shown that the genome of one of these species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid), with a further study suggesting that M. incognita may be the result of multiple additive hybridisation events: a hybrid of a hybrid. To understand the impact of allopolyploidy on plasticity, Blanc-Mathieu et al. resequenced the M. incognota genome and transcriptome (4 life stages) and sequenced the genomes of 2 related mitotic parthenogens, M. javanica and M. arenaria. These data were compared to existing assemblies of the meiotic parthenogen M. floridensis and the facultative sexually reproducing M. hapla

Jones, John T.

University of Dundee Online Publications

                                                                    University of DundeeSexEves-van den Akker, Sebastian; Jones, John T.Published in:PLoS GeneticsDOI:10.1371/journal.pgen.1007160Publication date:2018Licence:CC BYDocument VersionPublisher's PDF, also known as Version of recordLink to publication in Discovery Research PortalCitation for published version (APA):Eves-van den Akker, S., & Jones, J. T. (2018). Sex: Not all that it's cracked up to be? PLoS Genetics, 14(2), 1-4.[e1007160]. https://doi.org/10.1371/journal.pgen.1007160General rightsCopyright and moral rights for the publications made accessible in Discovery Research Portal are retained by the authors and/or othercopyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated withthese rights. • Users may download and print one copy of any publication from Discovery Research Portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain. • You may freely distribute the URL identifying the publication in the public portal.Take down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Download date: 19. Apr. 2023PERSPECTIVESex: Not all that it’s cracked up to be?Sebastian Eves-van den Akker1,2*, John T. Jones3,4*1 Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, United Kingdom, 2 School ofLife Sciences, University of Dundee, Dundee, United Kingdom, 3 Cell and Molecular Sciences Group,Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom, 4 School of Biology,University of St Andrews, North Haugh, St Andrews, United Kingdom* s.evesvandenakker@dundee.ac.uk (SEVDA); john.jones@hutton.ac.uk (JTJ)While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, thereare a small number of organisms that are testament to the contrary. The root-knot nematodesMeloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic partheno-genesis but have a broader host range, a wider geographical distribution, and a greater agricul-tural impact than their sexual relatives (Fig 1) [1]. Remarkably, some of these species even havethe ability to overcome host resistance [2], suggesting a mechanism for adaptation in the absenceof sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fullyunderstood. Previous genome sequencing of Meloidogyne has shown that the genome of one ofthese species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid),with a further study suggesting that M. incognita may be the result of multiple additive hybridisa-tion events: a hybrid of a hybrid [4].To understand the impact of allopolyploidy on plasticity, Blanc-Mathieu et al. [5] rese-quenced the M. incognota genome and transcriptome (4 life stages) and sequenced thegenomes of 2 related mitotic parthenogens, M. javanica and M. arenaria. These data werecompared to existing assemblies of the meiotic parthenogen M. floridensis and the facultativesexually reproducing M. hapla.Bewildering complexityAs expected, 89% of coding sequences in the sexual M. hapla align to a single locus in thegenome (>95% identity across2/3 of length), while in contrast, >85% of the codingsequences in the parthenogens M. incognita, M. javanica, and M. arenaria align to at least 2loci, but often more. Assuming the number of alignments is a rough proxy for copy number,M. incognita and M. javanica have more genes with at least 3 copies than any other copy num-ber. For M. arenaria, this phenomenon is further pronounced: more genes have at least 4 cop-ies than any other copy number. Blanc-Mathieu et al. [5] show that multicopy genome regionshave different evolutionary histories and thus support multiple different hybridisation events.Following a sudden gain in ploidy, one of each gene copy can often be lost, but this does notseem to have been the case yet in relatively “young” Meloidogyne species; only 4%–6% of ances-tral collinear genes seem to have been lost after the whole genome duplication event, and mostof the coding potential of each genome has therefore been retained. The end result is that thecoding potential is enormous: up to 100,000 predicted loci. In addition, compared to othernematode genomes, those of the mitotic parthenogens also contain an extremely high propor-tion of transposable elements (up to 50% of the genome). Given that transposable element pre-dictions wholly include 27%–30% of predicted protein-coding loci, the authors suggest that thismay have an adaptive impact, although recent phylum-wide analysis suggests that drift andPLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 1 / 4a1111111111a1111111111a1111111111a1111111111a1111111111OPENACCESSCitation: Eves-van den Akker S, Jones JT (2018)Sex: Not all that it’s cracked up to be? PLoS Genet14(2): e1007160. https://doi.org/10.1371/journal.pgen.1007160Editor: Takashi Gojobori, National Institute ofGenetics, JAPANPublished: February 22, 2018Copyright: © 2018 Eves-van den Akker, Jones. Thisis an open access article distributed under theterms of the Creative Commons AttributionLicense, which permits unrestricted use,distribution, and reproduction in any medium,provided the original author and source arecredited.Funding: This work was funded through RESASStrategic Research Programme Workpackage 2.1and BBSRC award BB/M014207/1. The fundershad no role in study design, data collection andanalysis, decision to publish, or preparation of themanuscript.Competing interests: The authors have declaredthat no competing interests exist.PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 2 / 4purifying selection, not life history, determine transposable element evolution in Nematoda [6].However, several mechanisms were identified that may allow a significant adaptive impact: (1)multicopy loci are on average approximately 8% sequence divergent; (2) genes in the majorityof the expressed homologous gene pairs were assigned to different expression clusters (64%);and (3) gene pairs showing signs of diversifying selection are more often present in different dif-ferential expression clusters to one another than those with signs of purifying selection.The stage is setIt will now be possible to explore how the sequence divergence and apparent functional diver-gence of homologous gene copies relate to the parasitic lifestyle. Analysis of differential expres-sion—and, indeed, differential alternative splicing of homologous gene copies across the hostrange of M. incognita may provide a tangible link between the enormous apparent codingpotential and host range. It is worth noting that, assuming the parents of the hybridisationevents that gave rise to these Meloidogyne were not homozygous at every allele, an additionallevel of allelic variation is yet to be explored. It is not clear to what extent mitotic recombina-tion may have contributed to introducing heterogeneity, removing deleterious mutations, andfixing adaptive mutations immediately after the hybridisation event or more recently. Haplo-type sequencing may provide an answer to some of these questions in the future.One question that needs to be resolved is to what extent the genomes sequenced to date [5]are representative of the species. Following the loss of sexual reproduction, there is presumablyno genetic exchange between individuals, and thus, in terms of gene flow, each individual canbe conceptually regarded as a separate species. Given that recombination has clearly takenplace in the genomes of the mitotic parthenogens [5], comparing the genomes of isolates thathave reproduced under different selection pressures would be fascinating. Because of the geneflow barrier imposed by abandoning sex, these need not necessarily be geographically distinct;nevertheless, it would be interesting to explore the impact of prolonged exposure to differenthosts and environments on genome evolution. Sequencing several geographically separatedisolates may also help to explain the apparent contradiction of a relatively recent evolutionaryorigin but worldwide distribution of these species (Fig 1).Finally, it is thought that the ability of a parasite to manipulate its host is due to the activitiesof effectors: secreted molecules that are delivered into the host during infection. The effectorcomplement of the tropical root-knot nematodes was not explored in the present study. Consid-ering the often unusual genome evolution of effectors (reviewed in [7]), analysing the arrange-ment, expression, regulation, and diversity of effectors in the polyploid Meloidogyne would beintriguing. It has been suggested that the success of M. incognita is consistent with the phenom-enon of transgressive segregation [4]: hybrids often outperform their parents for a given pheno-type. How transgressive segregation scales with multiple (additive) hybridisation events isunclear, but this may explain a host range that encompasses almost every flowering plant.AcknowledgmentsThe authors thank Peter J. Cock for mining taxonomy information.Fig 1. Geographical distribution and host range of M. incognita. Information from the Cookies on Invasive SpeciesCompendium (CABI) data sheet (https://www.cabi.org/isc/datasheet/33245; accessed 23 November 2017). All data arenonexhaustive; the absence of evidence is not evidence of absence. (A) Geographical distribution. (B) Partialphylogenetic time tree of plants (timetree.org; accessed 23 November 2017). Red indicates orders with at least 1, butoften more, host species. The extraordinarily broad host range of M. incognita covers most orders in the floweringplants (Magnoliophyta) but is apparently restricted to flowering plants—although this may reflect testing bias.https://doi.org/10.1371/journal.pgen.1007160.g001PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 3 / 4References1. Trudgill DL, Blok VC. Apomictic, polyphagous root-knot nematodes: exceptionally successful and dam-aging biotrophic root pathogens. Annu Rev Phytopathol. 2001; 39(1):53–77.2. Castagnone-Sereno P. Genetic variability and adaptive evolution in parthenogenetic root-knot nema-todes. Heredity. 2006; 96(4):282–9. https://doi.org/10.1038/sj.hdy.6800794 PMID: 164044123. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. Genome sequenceof the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol. 2008; 26(8):909–15.https://doi.org/10.1038/nbt.1482 PMID: 186608044. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. The complex hybrid origins of the root knot nematodesrevealed through comparative genomics. PeerJ. 2014; 2:e356. https://doi.org/10.7717/peerj.356 PMID:248606955. Blanc-Mathieu R, Perfus-Barbeoch L, Aury J-M, Da Rocha M, Gouzy J, Sallet E, et al. Hybridization andpolyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes.PLoS Genet. 2017; 13(6):e1006777. https://doi.org/10.1371/journal.pgen.1006777 PMID: 285948226. Szitenberg A, Cha S, Opperman CH, Bird DM, Blaxter ML, Lunt DH. Genetic drift, not life history orRNAi, determine long-term evolution of transposable elements. Genome biology and evolution. 2016; 8(9):2964–78. https://doi.org/10.1093/gbe/evw208 PMID: 275667627. Kikuchi T, Eves-van den Akker S, Jones JT. Genome Evolution of Plant-Parasitic Nematodes. AnnuRev Phytopathol. 2017; 55(1).PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 4 / 4

Sex:Not all that it's cracked up to be?

University of St. Andrews - Pure

Sex:not all that it’s cracked up to be?

                                                              University of DundeeSexEves-van den Akker, Sebastian; Jones, John T.Published in:PLoS GeneticsDOI:10.1371/journal.pgen.1007160Publication date:2018Document VersionPublisher's PDF, also known as Version of recordLink to publication in Discovery Research PortalCitation for published version (APA):Eves-van den Akker, S., & Jones, J. T. (2018). Sex: Not all that it's cracked up to be? PLoS Genetics, 14(2), 1-4.[e1007160]. DOI: 10.1371/journal.pgen.1007160General rightsCopyright and moral rights for the publications made accessible in Discovery Research Portal are retained by the authors and/or othercopyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated withthese rights. • Users may download and print one copy of any publication from Discovery Research Portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain. • You may freely distribute the URL identifying the publication in the public portal.Take down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Download date: 20. Mar. 2018PERSPECTIVESex: Not all that it’s cracked up to be?Sebastian Eves-van den Akker1,2*, John T. Jones3,4*1 Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, United Kingdom, 2 School ofLife Sciences, University of Dundee, Dundee, United Kingdom, 3 Cell and Molecular Sciences Group,Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom, 4 School of Biology,University of St Andrews, North Haugh, St Andrews, United Kingdom* s.evesvandenakker@dundee.ac.uk (SEVDA); john.jones@hutton.ac.uk (JTJ)While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, thereare a small number of organisms that are testament to the contrary. The root-knot nematodesMeloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic partheno-genesis but have a broader host range, a wider geographical distribution, and a greater agricul-tural impact than their sexual relatives (Fig 1) [1]. Remarkably, some of these species even havethe ability to overcome host resistance [2], suggesting a mechanism for adaptation in the absenceof sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fullyunderstood. Previous genome sequencing of Meloidogyne has shown that the genome of one ofthese species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid),with a further study suggesting that M. incognita may be the result of multiple additive hybridisa-tion events: a hybrid of a hybrid [4].To understand the impact of allopolyploidy on plasticity, Blanc-Mathieu et al. [5] rese-quenced the M. incognota genome and transcriptome (4 life stages) and sequenced thegenomes of 2 related mitotic parthenogens, M. javanica and M. arenaria. These data werecompared to existing assemblies of the meiotic parthenogen M. floridensis and the facultativesexually reproducing M. hapla.Bewildering complexityAs expected, 89% of coding sequences in the sexual M. hapla align to a single locus in thegenome (>95% identity across2/3 of length), while in contrast, >85% of the codingsequences in the parthenogens M. incognita, M. javanica, and M. arenaria align to at least 2loci, but often more. Assuming the number of alignments is a rough proxy for copy number,M. incognita and M. javanica have more genes with at least 3 copies than any other copy num-ber. For M. arenaria, this phenomenon is further pronounced: more genes have at least 4 cop-ies than any other copy number. Blanc-Mathieu et al. [5] show that multicopy genome regionshave different evolutionary histories and thus support multiple different hybridisation events.Following a sudden gain in ploidy, one of each gene copy can often be lost, but this does notseem to have been the case yet in relatively “young” Meloidogyne species; only 4%–6% of ances-tral collinear genes seem to have been lost after the whole genome duplication event, and mostof the coding potential of each genome has therefore been retained. The end result is that thecoding potential is enormous: up to 100,000 predicted loci. In addition, compared to othernematode genomes, those of the mitotic parthenogens also contain an extremely high propor-tion of transposable elements (up to 50% of the genome). Given that transposable element pre-dictions wholly include 27%–30% of predicted protein-coding loci, the authors suggest that thismay have an adaptive impact, although recent phylum-wide analysis suggests that drift andPLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 1 / 4a1111111111a1111111111a1111111111a1111111111a1111111111OPENACCESSCitation: Eves-van den Akker S, Jones JT (2018)Sex: Not all that it’s cracked up to be? PLoS Genet14(2): e1007160. https://doi.org/10.1371/journal.pgen.1007160Editor: Takashi Gojobori, National Institute ofGenetics, JAPANPublished: February 22, 2018Copyright: © 2018 Eves-van den Akker, Jones. Thisis an open access article distributed under theterms of the Creative Commons AttributionLicense, which permits unrestricted use,distribution, and reproduction in any medium,provided the original author and source arecredited.Funding: This work was funded through RESASStrategic Research Programme Workpackage 2.1and BBSRC award BB/M014207/1. The fundershad no role in study design, data collection andanalysis, decision to publish, or preparation of themanuscript.Competing interests: The authors have declaredthat no competing interests exist.PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 2 / 4purifying selection, not life history, determine transposable element evolution in Nematoda [6].However, several mechanisms were identified that may allow a significant adaptive impact: (1)multicopy loci are on average approximately 8% sequence divergent; (2) genes in the majorityof the expressed homologous gene pairs were assigned to different expression clusters (64%);and (3) gene pairs showing signs of diversifying selection are more often present in different dif-ferential expression clusters to one another than those with signs of purifying selection.The stage is setIt will now be possible to explore how the sequence divergence and apparent functional diver-gence of homologous gene copies relate to the parasitic lifestyle. Analysis of differential expres-sion—and, indeed, differential alternative splicing of homologous gene copies across the hostrange of M. incognita may provide a tangible link between the enormous apparent codingpotential and host range. It is worth noting that, assuming the parents of the hybridisationevents that gave rise to these Meloidogyne were not homozygous at every allele, an additionallevel of allelic variation is yet to be explored. It is not clear to what extent mitotic recombina-tion may have contributed to introducing heterogeneity, removing deleterious mutations, andfixing adaptive mutations immediately after the hybridisation event or more recently. Haplo-type sequencing may provide an answer to some of these questions in the future.One question that needs to be resolved is to what extent the genomes sequenced to date [5]are representative of the species. Following the loss of sexual reproduction, there is presumablyno genetic exchange between individuals, and thus, in terms of gene flow, each individual canbe conceptually regarded as a separate species. Given that recombination has clearly takenplace in the genomes of the mitotic parthenogens [5], comparing the genomes of isolates thathave reproduced under different selection pressures would be fascinating. Because of the geneflow barrier imposed by abandoning sex, these need not necessarily be geographically distinct;nevertheless, it would be interesting to explore the impact of prolonged exposure to differenthosts and environments on genome evolution. Sequencing several geographically separatedisolates may also help to explain the apparent contradiction of a relatively recent evolutionaryorigin but worldwide distribution of these species (Fig 1).Finally, it is thought that the ability of a parasite to manipulate its host is due to the activitiesof effectors: secreted molecules that are delivered into the host during infection. The effectorcomplement of the tropical root-knot nematodes was not explored in the present study. Consid-ering the often unusual genome evolution of effectors (reviewed in [7]), analysing the arrange-ment, expression, regulation, and diversity of effectors in the polyploid Meloidogyne would beintriguing. It has been suggested that the success of M. incognita is consistent with the phenom-enon of transgressive segregation [4]: hybrids often outperform their parents for a given pheno-type. How transgressive segregation scales with multiple (additive) hybridisation events isunclear, but this may explain a host range that encompasses almost every flowering plant.AcknowledgmentsThe authors thank Peter J. Cock for mining taxonomy information.Fig 1. Geographical distribution and host range of M. incognita. Information from the Cookies on Invasive SpeciesCompendium (CABI) data sheet (https://www.cabi.org/isc/datasheet/33245; accessed 23 November 2017). All data arenonexhaustive; the absence of evidence is not evidence of absence. (A) Geographical distribution. (B) Partialphylogenetic time tree of plants (timetree.org; accessed 23 November 2017). Red indicates orders with at least 1, butoften more, host species. The extraordinarily broad host range of M. incognita covers most orders in the floweringplants (Magnoliophyta) but is apparently restricted to flowering plants—although this may reflect testing bias.https://doi.org/10.1371/journal.pgen.1007160.g001PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 3 / 4References1. Trudgill DL, Blok VC. Apomictic, polyphagous root-knot nematodes: exceptionally successful and dam-aging biotrophic root pathogens. Annu Rev Phytopathol. 2001; 39(1):53–77.2. Castagnone-Sereno P. Genetic variability and adaptive evolution in parthenogenetic root-knot nema-todes. Heredity. 2006; 96(4):282–9. https://doi.org/10.1038/sj.hdy.6800794 PMID: 164044123. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. Genome sequenceof the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol. 2008; 26(8):909–15.https://doi.org/10.1038/nbt.1482 PMID: 186608044. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. The complex hybrid origins of the root knot nematodesrevealed through comparative genomics. PeerJ. 2014; 2:e356. https://doi.org/10.7717/peerj.356 PMID:248606955. Blanc-Mathieu R, Perfus-Barbeoch L, Aury J-M, Da Rocha M, Gouzy J, Sallet E, et al. Hybridization andpolyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes.PLoS Genet. 2017; 13(6):e1006777. https://doi.org/10.1371/journal.pgen.1006777 PMID: 285948226. Szitenberg A, Cha S, Opperman CH, Bird DM, Blaxter ML, Lunt DH. Genetic drift, not life history orRNAi, determine long-term evolution of transposable elements. Genome biology and evolution. 2016; 8(9):2964–78. https://doi.org/10.1093/gbe/evw208 PMID: 275667627. Kikuchi T, Eves-van den Akker S, Jones JT. Genome Evolution of Plant-Parasitic Nematodes. AnnuRev Phytopathol. 2017; 55(1).PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 4 / 4

Sebastian Eves-van den Akker

John T. Jones

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Sex: Not all that it’s cracked up to be?

John T Jones

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Sex: Not all that it's cracked up to be?

This work was funded through RESAS Strategic Research Programme Workpackage 2.1 and BBSRC award BB/M014207/1.Publisher PDFPeer reviewe

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PERSPECTIVESex: Not all that it’s cracked up to be?Sebastian Eves-van den Akker1,2*, John T. Jones3,4*1 Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, United Kingdom, 2 School ofLife Sciences, University of Dundee, Dundee, United Kingdom, 3 Cell and Molecular Sciences Group,Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom, 4 School of Biology,University of St Andrews, North Haugh, St Andrews, United Kingdom* s.evesvandenakker@dundee.ac.uk (SEVDA); john.jones@hutton.ac.uk (JTJ)While sexual reproduction is generally thought to be, evolutionarily speaking, a good idea, thereare a small number of organisms that are testament to the contrary. The root-knot nematodesMeloidogyne incognita, M. javanica, and M. arenaria reproduce clonally using mitotic partheno-genesis but have a broader host range, a wider geographical distribution, and a greater agricul-tural impact than their sexual relatives (Fig 1) [1]. Remarkably, some of these species even havethe ability to overcome host resistance [2], suggesting a mechanism for adaptation in the absenceof sex. The genetic basis of this plasticity, both in terms of host range and adaptability, is not fullyunderstood. Previous genome sequencing of Meloidogyne has shown that the genome of one ofthese species, M. incognita, is polyploid [3], most likely as a result of hybridisation (allopolyploid),with a further study suggesting that M. incognita may be the result of multiple additive hybridisa-tion events: a hybrid of a hybrid [4].To understand the impact of allopolyploidy on plasticity, Blanc-Mathieu et al. [5] rese-quenced the M. incognota genome and transcriptome (4 life stages) and sequenced thegenomes of 2 related mitotic parthenogens, M. javanica and M. arenaria. These data werecompared to existing assemblies of the meiotic parthenogen M. floridensis and the facultativesexually reproducing M. hapla.Bewildering complexityAs expected, 89% of coding sequences in the sexual M. hapla align to a single locus in thegenome (>95% identity across2/3 of length), while in contrast, >85% of the codingsequences in the parthenogens M. incognita, M. javanica, and M. arenaria align to at least 2loci, but often more. Assuming the number of alignments is a rough proxy for copy number,M. incognita and M. javanica have more genes with at least 3 copies than any other copy num-ber. For M. arenaria, this phenomenon is further pronounced: more genes have at least 4 cop-ies than any other copy number. Blanc-Mathieu et al. [5] show that multicopy genome regionshave different evolutionary histories and thus support multiple different hybridisation events.Following a sudden gain in ploidy, one of each gene copy can often be lost, but this does notseem to have been the case yet in relatively “young” Meloidogyne species; only 4%–6% of ances-tral collinear genes seem to have been lost after the whole genome duplication event, and mostof the coding potential of each genome has therefore been retained. The end result is that thecoding potential is enormous: up to 100,000 predicted loci. In addition, compared to othernematode genomes, those of the mitotic parthenogens also contain an extremely high propor-tion of transposable elements (up to 50% of the genome). Given that transposable element pre-dictions wholly include 27%–30% of predicted protein-coding loci, the authors suggest that thismay have an adaptive impact, although recent phylum-wide analysis suggests that drift andPLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 1 / 4a1111111111a1111111111a1111111111a1111111111a1111111111OPENACCESSCitation: Eves-van den Akker S, Jones JT (2018)Sex: Not all that it’s cracked up to be? PLoS Genet14(2): e1007160. https://doi.org/10.1371/journal.pgen.1007160Editor: Takashi Gojobori, National Institute ofGenetics, JAPANPublished: February 22, 2018Copyright: © 2018 Eves-van den Akker, Jones. Thisis an open access article distributed under theterms of the Creative Commons AttributionLicense, which permits unrestricted use,distribution, and reproduction in any medium,provided the original author and source arecredited.Funding: This work was funded through RESASStrategic Research Programme Workpackage 2.1and BBSRC award BB/M014207/1. The fundershad no role in study design, data collection andanalysis, decision to publish, or preparation of themanuscript.Competing interests: The authors have declaredthat no competing interests exist.PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 2 / 4purifying selection, not life history, determine transposable element evolution in Nematoda [6].However, several mechanisms were identified that may allow a significant adaptive impact: (1)multicopy loci are on average approximately 8% sequence divergent; (2) genes in the majorityof the expressed homologous gene pairs were assigned to different expression clusters (64%);and (3) gene pairs showing signs of diversifying selection are more often present in different dif-ferential expression clusters to one another than those with signs of purifying selection.The stage is setIt will now be possible to explore how the sequence divergence and apparent functional diver-gence of homologous gene copies relate to the parasitic lifestyle. Analysis of differential expres-sion—and, indeed, differential alternative splicing of homologous gene copies across the hostrange of M. incognita may provide a tangible link between the enormous apparent codingpotential and host range. It is worth noting that, assuming the parents of the hybridisationevents that gave rise to these Meloidogyne were not homozygous at every allele, an additionallevel of allelic variation is yet to be explored. It is not clear to what extent mitotic recombina-tion may have contributed to introducing heterogeneity, removing deleterious mutations, andfixing adaptive mutations immediately after the hybridisation event or more recently. Haplo-type sequencing may provide an answer to some of these questions in the future.One question that needs to be resolved is to what extent the genomes sequenced to date [5]are representative of the species. Following the loss of sexual reproduction, there is presumablyno genetic exchange between individuals, and thus, in terms of gene flow, each individual canbe conceptually regarded as a separate species. Given that recombination has clearly takenplace in the genomes of the mitotic parthenogens [5], comparing the genomes of isolates thathave reproduced under different selection pressures would be fascinating. Because of the geneflow barrier imposed by abandoning sex, these need not necessarily be geographically distinct;nevertheless, it would be interesting to explore the impact of prolonged exposure to differenthosts and environments on genome evolution. Sequencing several geographically separatedisolates may also help to explain the apparent contradiction of a relatively recent evolutionaryorigin but worldwide distribution of these species (Fig 1).Finally, it is thought that the ability of a parasite to manipulate its host is due to the activitiesof effectors: secreted molecules that are delivered into the host during infection. The effectorcomplement of the tropical root-knot nematodes was not explored in the present study. Consid-ering the often unusual genome evolution of effectors (reviewed in [7]), analysing the arrange-ment, expression, regulation, and diversity of effectors in the polyploid Meloidogyne would beintriguing. It has been suggested that the success of M. incognita is consistent with the phenom-enon of transgressive segregation [4]: hybrids often outperform their parents for a given pheno-type. How transgressive segregation scales with multiple (additive) hybridisation events isunclear, but this may explain a host range that encompasses almost every flowering plant.AcknowledgmentsThe authors thank Peter J. Cock for mining taxonomy information.Fig 1. Geographical distribution and host range of M. incognita. Information from the Cookies on Invasive SpeciesCompendium (CABI) data sheet (https://www.cabi.org/isc/datasheet/33245; accessed 23 November 2017). All data arenonexhaustive; the absence of evidence is not evidence of absence. (A) Geographical distribution. (B) Partialphylogenetic time tree of plants (timetree.org; accessed 23 November 2017). Red indicates orders with at least 1, butoften more, host species. The extraordinarily broad host range of M. incognita covers most orders in the floweringplants (Magnoliophyta) but is apparently restricted to flowering plants—although this may reflect testing bias.https://doi.org/10.1371/journal.pgen.1007160.g001PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 3 / 4References1. Trudgill DL, Blok VC. Apomictic, polyphagous root-knot nematodes: exceptionally successful and dam-aging biotrophic root pathogens. Annu Rev Phytopathol. 2001; 39(1):53–77.2. Castagnone-Sereno P. Genetic variability and adaptive evolution in parthenogenetic root-knot nema-todes. Heredity. 2006; 96(4):282–9. https://doi.org/10.1038/sj.hdy.6800794 PMID: 164044123. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. Genome sequenceof the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol. 2008; 26(8):909–15.https://doi.org/10.1038/nbt.1482 PMID: 186608044. Lunt DH, Kumar S, Koutsovoulos G, Blaxter ML. The complex hybrid origins of the root knot nematodesrevealed through comparative genomics. PeerJ. 2014; 2:e356. https://doi.org/10.7717/peerj.356 PMID:248606955. Blanc-Mathieu R, Perfus-Barbeoch L, Aury J-M, Da Rocha M, Gouzy J, Sallet E, et al. Hybridization andpolyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes.PLoS Genet. 2017; 13(6):e1006777. https://doi.org/10.1371/journal.pgen.1006777 PMID: 285948226. Szitenberg A, Cha S, Opperman CH, Bird DM, Blaxter ML, Lunt DH. Genetic drift, not life history orRNAi, determine long-term evolution of transposable elements. Genome biology and evolution. 2016; 8(9):2964–78. https://doi.org/10.1093/gbe/evw208 PMID: 275667627. Kikuchi T, Eves-van den Akker S, Jones JT. Genome Evolution of Plant-Parasitic Nematodes. AnnuRev Phytopathol. 2017; 55(1).PLOS Genetics | https://doi.org/10.1371/journal.pgen.1007160 February 22, 2018 4 / 4

Sex : not all that it’s cracked up to be?

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Sex: Not all that it's cracked up to be?

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