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Intergenomic Arms Races: Detection of a Nuclear Rescue Gene of Male-Killing in a Ladybird


Many species of arthropod are infected by deleterious inherited micro-organisms. Typically these micro-organisms are inherited maternally. Consequently, some, particularly bacteria of the genus Wolbachia, employ a variety of strategies that favour female over male hosts. These strategies include feminisation, induction of parthenogenesis and male-killing. These strategies result in female biased sex ratios in host populations, which lead to selection for host factors that promote male production. In addition, the intra-genomic conflict produced by the difference in transmission of these cytoplasmic endosymbionts and nuclear factors will impose a pressure favouring nuclear factors that suppress the effects of the symbiont. During investigations of the diversity of male-killing bacteria in ladybirds (Coccinellidae), unexpected patterns of vertical transmission of a newly discovered male-killing taxon were observed in the ladybird Cheilomenes sexmaculata. Initial analysis suggested that the expression of the bacterial male-killing trait varies according to the male(s) a female has mated with. By swapping males between females, a male influence on the expression of the male-killing trait was confirmed. Experiments were then performed to determine the nature of the interaction. These studies showed that a single dominant allele, which rescues male progeny of infected females from the pathological effect of the male-killer, exists in this species. The gene shows typical Mendelian autosomal inheritance and is expressed irrespective of the parent from which it is inherited. Presence of the rescue gene in either parent does not significantly affect the inheritance of the symbiont. We conclude that C. sexmaculata is host to a male-killing γ-proteobacterium. Further, this beetle is polymorphic for a nuclear gene, the dominant allele of which rescues infected males from the pathogenic effects of the male-killing agent. These findings represent the first reported case of a nuclear suppressor of male-killing in a ladybird. They are considered in regard to sex ratio and intra-genomic conflict theories, and models of the evolutionary dynamics and distribution of inherited symbionts.


Vyšlo v časopise: Intergenomic Arms Races: Detection of a Nuclear Rescue Gene of Male-Killing in a Ladybird. PLoS Pathog 6(7): e32767. doi:10.1371/journal.ppat.1000987
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000987

Souhrn

Many species of arthropod are infected by deleterious inherited micro-organisms. Typically these micro-organisms are inherited maternally. Consequently, some, particularly bacteria of the genus Wolbachia, employ a variety of strategies that favour female over male hosts. These strategies include feminisation, induction of parthenogenesis and male-killing. These strategies result in female biased sex ratios in host populations, which lead to selection for host factors that promote male production. In addition, the intra-genomic conflict produced by the difference in transmission of these cytoplasmic endosymbionts and nuclear factors will impose a pressure favouring nuclear factors that suppress the effects of the symbiont. During investigations of the diversity of male-killing bacteria in ladybirds (Coccinellidae), unexpected patterns of vertical transmission of a newly discovered male-killing taxon were observed in the ladybird Cheilomenes sexmaculata. Initial analysis suggested that the expression of the bacterial male-killing trait varies according to the male(s) a female has mated with. By swapping males between females, a male influence on the expression of the male-killing trait was confirmed. Experiments were then performed to determine the nature of the interaction. These studies showed that a single dominant allele, which rescues male progeny of infected females from the pathological effect of the male-killer, exists in this species. The gene shows typical Mendelian autosomal inheritance and is expressed irrespective of the parent from which it is inherited. Presence of the rescue gene in either parent does not significantly affect the inheritance of the symbiont. We conclude that C. sexmaculata is host to a male-killing γ-proteobacterium. Further, this beetle is polymorphic for a nuclear gene, the dominant allele of which rescues infected males from the pathogenic effects of the male-killing agent. These findings represent the first reported case of a nuclear suppressor of male-killing in a ladybird. They are considered in regard to sex ratio and intra-genomic conflict theories, and models of the evolutionary dynamics and distribution of inherited symbionts.


Zdroje

1. WerrenJH

O'NeillSL

1997 The evolution of heritable symbionts.

O'NeillSL

HoffmannAA

WerrenJH

Influential Passengers Oxford Oxford University Press 1 41

2. MajerusMEN

HurstGDD

1997 Ladybirds as a model system for the study of male-killing symbionts. Entomophaga 42 13 20

3. HurstGDD

HurstLD

MajerusMEN

1997 Cytoplasmic sex-ratio distorters.

O'NeillSL

HoffmannAA

WerrenJH

Influential Passengers Oxford Oxford University Press 125 154

4. WerrenJH

1987 The coevolution of autosomal and cytoplasmic sex ratio factors. J Theor Biol 124 317 334

5. HurstLD

1992 Intragenomic conflict as an evolutionary force. P Roy Soc Lond B Bio 248 91 99

6. OwenDF

ChanterDO

1969 Population biology of tropical African butterflies. Sex ratio and genetic variation in Acraea encedon. J Zool 157 345 374

7. MajerusMEN

MajerusTMO

2000 Female-biased sex ratio due to male-killing in the Japanese ladybird Coccinula sinensis. Ecol Entomol 25 234 238

8. UyenoyamaMK

FeldmanMW

1978 The genetics of sex ratio distortion by cytoplasmic infection under maternal and contagious transmission: an epidemiological study. Theor Popul Biol 14 471 497

9. FrankSA

1989 The evolutionary dynamics of cytoplasmic male sterility. Am Nat 133 345 376

10. MerçotH

LlorenteB

JacquesM

AtlanA

Montchamp-MoreauC

1995 Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics 141 1015 1023

11. JuchaultP

FrelonM

BouchonD

RigaudT

1994 New evidence for feminizing bacteria in terrestrial isopods: evolutionary implications. C R Acad Sci Paris, Série III 317 225 230

12. CavalcantiAGL

FalcaoDN

CastroLE

1957 “Sex-ratio” in Drosophila prosaltans- a character due to interaction between nuclear genes and cytoplasmic factors. Am Nat 91 327 329

13. HornettEA

CharlatS

DuplouyAMR

DaviesN

RoderickGK

2006 Evolution of Male-Killer Suppression in a Natural Population. PLoS Biol 4 e283

14. WeinertLA

TinsleyMC

TemperleyM

JigginsFM

2007 Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol Lett 3 678 681

15. JaenikeJ

2007 Spontaneous emergence of a new Wolbachia phenotype. Evolution 61 2244 2252

16. SasakiT

KuboT

IshikawaH

2002 Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics 162 1313 1319

17. NiijimaK

NakajimaK

1981 Abnormal sex ratio in Menochilus sexmaculatus (Fabricius). B Fac Agr Tamagawa U 21 59 67

18. GotohT

NiijimaK

1986 Characteristics and agent(s) of abnormal sex ratio (SR) in two aphidophagous coccinellid species.

HodekI

Ecology of the Aphidophaga Prague Academia 545 550

19. MajerusTMO

SchulenburgJHGvd

MajerusMEN

HurstGDD

1999 Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8 551 555

20. WeisbergWG

BarnsSM

PelletierDA

LaneDJ

1991 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173 697 703

21. HurstGDD

JigginsFM

SchulenbergJHGvd

BertrandD

WestSA

1999 Male-killing Wolbachia in two species of insect. P Roy Soc Lond B Bio 266 735 740

22. ZhangZ

SchwartzS

WagnerL

MillerW

2000 A greedy algorithm for aligning DNA sequences. J Comput Biol 7 203 14

23. SandstromJP

RussellJA

WhiteJP

MoranNA

2001 Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10 217 228

24. RussellJA

LatorreA

Sabater-MunozB

MoyaA

MoranNA

2003 Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12 1061 1075

25. OliverKM

DegnanPH

BurkeGR

MoranNA

Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55 247 66

26. MajerusTMO

MajerusMEN

2010 Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae). BMC Evol Biol 10 37

27. MajerusTMO

2001 The Evolutionary Genetics of Male killing in the Coccinellidae. PhD thesis. University of Cambridge, Department of Genetics

28. HedgesLM

BrownlieJC

O'NeillSL

JohnsonKN

2008 Wolbachia and virus protection in insects. Science 322 702

29. GhernaRL

WerrenJH

WeisburgW

CoteR

WoeseCR

1991 Arsenophonus nasoniae, genus novel, species novel, causative agent of Son Killer trait in the parasitic wasp, Nasonia vitripennis. Int J Syst Bacteriol 41 563 565

30. FisherRA

1930 The Genetical Theory of Natural Selection. Oxford Oxford University Press 318

31. HamiltonWD

1967 Extraordinary sex ratios. Science 156 477 488

32. RigaudT

JuchaultP

1992 Genetic control of the vertical transmission of a cytoplasmic sex factor in Armadillium vulgare atr. (Crustacea, Oniscidea). Heredity 68 47 52

33. StouthamerR

1997 Wolbachia-induced parthenogenesis.

O'NeillSL

HoffmannAA

WerrenJH

Influential Passengers Oxford Oxford University Press 102 124

34. RandersonJP

SmithGC

HurstLD

2000 The evolutionary dynamics of male-killers and their hosts. Heredity 84 152 160

35. RigaudT

1997 Inherited microorganisms and sex determination of arthropod hosts.

O'NeillSL

HoffmannAA

WerrenJH

Influential Passengers Oxford Oxford University Press 81 101

36. HornettEA

EngelstädterJ

HurstGD

2010 Hidden cytoplasmic incompatibility alters the dynamics of male-killer/host interactions. J Evolution Biol 23 479 487

37. LaneDJ

PaceB

OlsenGJ

StahlDA

SoginML

1985 Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. P Natl Acad Sci U S A 82 6955 6959

38. LarkinMA

BlackshieldsG

BrownNP

ChennaR

McGettiganPA

2007 ClustalW and ClustalX version 2. Bioinformatics 23 2947 2948

39. GouyM

GuindonS

GascuelO

2010 SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27 221 224

40. PerrièreG

GouyM

1996 WWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78 364 369

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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