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Genetic control of contagious asexuality in the pea aphid.

Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, Bonhomme J, Mahéo F, Legeai F, Gauthier JP, Prunier-Leterme N, Tagu D, Simon JC - PLoS Genet. (2014)

Bottom Line: Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches.A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses.These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR1349, Institute of Genetics, Environment and Plant Protection, Domaine de la Motte, Le Rheu, France.

ABSTRACT
Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼ 300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.

No MeSH data available.


Localization of the genomic region controlling reproductive phenotype on genetic maps of the pea aphid.On these maps of each chromosome (LG1 to LG4), we show results from two independent approaches to identify genomic regions that control reproductive mode variation (i.e. the production of sexual females) in the pea aphid. 1) QTL approach: Likelihood ratio (LR) along chromosomes for the presence of a QTL are shown (solid blue curves correspond to LR values for % of sexual females, and solid black curves to LR values for occurrence of sexual females). The LR thresholds corresponding to a p-value of 0.05 at the genome-level (i.e. adjusted for multiple testing) are also shown (dashed blue line for % of sexual females and dashed black line for occurrence of sexual females). Threshold lines for the two traits are almost superimposed. The blue and black bars show the location of the 95% CI of the QTL for % of sexual females and occurrence of sexual females, respectively. 2) Population genomic approach: a hierarchical genome scan was performed using ARLEQUIN 3.5 to identify genomic regions involved in reproductive mode variation. The genetic differentiation values (FCT) among three OP and three CP populations are shown along chromosomes. Loci identified as significant outliers (hence candidate loci for reproductive mode variation) at 1%, 5% or 10% are shown in red, orange and yellow, respectively, and non-outlier markers with a cross. The black line corresponds to a moving average on FCT (calculated on a 15 cM window).
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pgen-1004838-g002: Localization of the genomic region controlling reproductive phenotype on genetic maps of the pea aphid.On these maps of each chromosome (LG1 to LG4), we show results from two independent approaches to identify genomic regions that control reproductive mode variation (i.e. the production of sexual females) in the pea aphid. 1) QTL approach: Likelihood ratio (LR) along chromosomes for the presence of a QTL are shown (solid blue curves correspond to LR values for % of sexual females, and solid black curves to LR values for occurrence of sexual females). The LR thresholds corresponding to a p-value of 0.05 at the genome-level (i.e. adjusted for multiple testing) are also shown (dashed blue line for % of sexual females and dashed black line for occurrence of sexual females). Threshold lines for the two traits are almost superimposed. The blue and black bars show the location of the 95% CI of the QTL for % of sexual females and occurrence of sexual females, respectively. 2) Population genomic approach: a hierarchical genome scan was performed using ARLEQUIN 3.5 to identify genomic regions involved in reproductive mode variation. The genetic differentiation values (FCT) among three OP and three CP populations are shown along chromosomes. Loci identified as significant outliers (hence candidate loci for reproductive mode variation) at 1%, 5% or 10% are shown in red, orange and yellow, respectively, and non-outlier markers with a cross. The black line corresponds to a moving average on FCT (calculated on a 15 cM window).

Mentions: We produced F1 crosses between males of an obligate parthenogenetic lineage (L21V1) and sexual females of two cyclically parthenogenetic lineages (JML06 and LSR1) (Fig. 1). Five F2 crosses (families 3 to 7) involving 6 F1 lineages were performed to obtain a genetic map and to locate QTL controlling the presence and proportion of sexual females by genotypes placed under sex-inducing conditions. A total of 305 microsatellite markers (out of 394) was successfully ordered on the genetic maps. These loci clustered in four linkage groups that correspond to the four chromosomes of the pea aphid [25]. 45 loci locate on the X chromosome (LG1 following notation in [26]), and 85, 135, and 40 on LG2, LG3 and LG4, respectively. Average map length (over males and females) was 113, 95, 79 and 59 cM for LG1, LG2, LG3 and LG4, respectively (Fig. 2). Of the 89 unmapped loci (out of 394), 51 were monomorphic in the 3-generation pedigree, five were homozygous in all F1 females, and 33 showed alleles at high frequencies or inconsistent genotypes (presumably due to difficulties to score alleles).


Genetic control of contagious asexuality in the pea aphid.

Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, Bonhomme J, Mahéo F, Legeai F, Gauthier JP, Prunier-Leterme N, Tagu D, Simon JC - PLoS Genet. (2014)

Localization of the genomic region controlling reproductive phenotype on genetic maps of the pea aphid.On these maps of each chromosome (LG1 to LG4), we show results from two independent approaches to identify genomic regions that control reproductive mode variation (i.e. the production of sexual females) in the pea aphid. 1) QTL approach: Likelihood ratio (LR) along chromosomes for the presence of a QTL are shown (solid blue curves correspond to LR values for % of sexual females, and solid black curves to LR values for occurrence of sexual females). The LR thresholds corresponding to a p-value of 0.05 at the genome-level (i.e. adjusted for multiple testing) are also shown (dashed blue line for % of sexual females and dashed black line for occurrence of sexual females). Threshold lines for the two traits are almost superimposed. The blue and black bars show the location of the 95% CI of the QTL for % of sexual females and occurrence of sexual females, respectively. 2) Population genomic approach: a hierarchical genome scan was performed using ARLEQUIN 3.5 to identify genomic regions involved in reproductive mode variation. The genetic differentiation values (FCT) among three OP and three CP populations are shown along chromosomes. Loci identified as significant outliers (hence candidate loci for reproductive mode variation) at 1%, 5% or 10% are shown in red, orange and yellow, respectively, and non-outlier markers with a cross. The black line corresponds to a moving average on FCT (calculated on a 15 cM window).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256089&req=5

pgen-1004838-g002: Localization of the genomic region controlling reproductive phenotype on genetic maps of the pea aphid.On these maps of each chromosome (LG1 to LG4), we show results from two independent approaches to identify genomic regions that control reproductive mode variation (i.e. the production of sexual females) in the pea aphid. 1) QTL approach: Likelihood ratio (LR) along chromosomes for the presence of a QTL are shown (solid blue curves correspond to LR values for % of sexual females, and solid black curves to LR values for occurrence of sexual females). The LR thresholds corresponding to a p-value of 0.05 at the genome-level (i.e. adjusted for multiple testing) are also shown (dashed blue line for % of sexual females and dashed black line for occurrence of sexual females). Threshold lines for the two traits are almost superimposed. The blue and black bars show the location of the 95% CI of the QTL for % of sexual females and occurrence of sexual females, respectively. 2) Population genomic approach: a hierarchical genome scan was performed using ARLEQUIN 3.5 to identify genomic regions involved in reproductive mode variation. The genetic differentiation values (FCT) among three OP and three CP populations are shown along chromosomes. Loci identified as significant outliers (hence candidate loci for reproductive mode variation) at 1%, 5% or 10% are shown in red, orange and yellow, respectively, and non-outlier markers with a cross. The black line corresponds to a moving average on FCT (calculated on a 15 cM window).
Mentions: We produced F1 crosses between males of an obligate parthenogenetic lineage (L21V1) and sexual females of two cyclically parthenogenetic lineages (JML06 and LSR1) (Fig. 1). Five F2 crosses (families 3 to 7) involving 6 F1 lineages were performed to obtain a genetic map and to locate QTL controlling the presence and proportion of sexual females by genotypes placed under sex-inducing conditions. A total of 305 microsatellite markers (out of 394) was successfully ordered on the genetic maps. These loci clustered in four linkage groups that correspond to the four chromosomes of the pea aphid [25]. 45 loci locate on the X chromosome (LG1 following notation in [26]), and 85, 135, and 40 on LG2, LG3 and LG4, respectively. Average map length (over males and females) was 113, 95, 79 and 59 cM for LG1, LG2, LG3 and LG4, respectively (Fig. 2). Of the 89 unmapped loci (out of 394), 51 were monomorphic in the 3-generation pedigree, five were homozygous in all F1 females, and 33 showed alleles at high frequencies or inconsistent genotypes (presumably due to difficulties to score alleles).

Bottom Line: Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches.A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses.These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR1349, Institute of Genetics, Environment and Plant Protection, Domaine de la Motte, Le Rheu, France.

ABSTRACT
Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼ 300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.

No MeSH data available.