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Michel Chapuisat - One of the best experts on this subject based on the ideXlab platform.
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maternal effect killing by a Supergene controlling ant social organization
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Amaury Avril, Sebastien Beniguel, Jessica Purcell, Michel ChapuisatAbstract:Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the Supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social Supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.
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An Ancient and Eroded Social Supergene Is Widespread across Formica Ants
Current biology : CB, 2020Co-Authors: Alan Brelsford, Amaury Avril, Jessica Purcell, Liselotte Sundström, Heikki Helanterä, Patrick Tran Van, Junxia Zhang, Timothée Brütsch, Michel ChapuisatAbstract:Summary Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [ 1 , 2 ]. Although Supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [ 3 ]. Here, we uncover 20–40 Ma of evolutionary history of a Supergene associated with polymorphic social organization in Formica ants [ 4 ]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the Supergene’s size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative Supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the Supergene. This unexpected pattern of divergence indicates that the Formica Supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [ 5 ]. We propose an alternative “eroded strata model” in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the Supergene contains a transcription factor essential for motor neuron development in Drosophila [ 6 ]. The discovery that a very small portion of this large and ancient Supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.
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asymmetric assortative mating and queen polyandry are linked to a Supergene controlling ant social organization
Molecular Ecology, 2019Co-Authors: Amaury Avril, Jessica Purcell, Alan Brelsford, Michel ChapuisatAbstract:Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these "social Supergenes" affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a Supergene with alternate haplotypes-Sm and Sp-underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male-mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the Supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.
Amaury Avril - One of the best experts on this subject based on the ideXlab platform.
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maternal effect killing by a Supergene controlling ant social organization
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Amaury Avril, Sebastien Beniguel, Jessica Purcell, Michel ChapuisatAbstract:Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the Supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social Supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.
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An Ancient and Eroded Social Supergene Is Widespread across Formica Ants
Current biology : CB, 2020Co-Authors: Alan Brelsford, Amaury Avril, Jessica Purcell, Liselotte Sundström, Heikki Helanterä, Patrick Tran Van, Junxia Zhang, Timothée Brütsch, Michel ChapuisatAbstract:Summary Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [ 1 , 2 ]. Although Supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [ 3 ]. Here, we uncover 20–40 Ma of evolutionary history of a Supergene associated with polymorphic social organization in Formica ants [ 4 ]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the Supergene’s size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative Supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the Supergene. This unexpected pattern of divergence indicates that the Formica Supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [ 5 ]. We propose an alternative “eroded strata model” in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the Supergene contains a transcription factor essential for motor neuron development in Drosophila [ 6 ]. The discovery that a very small portion of this large and ancient Supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.
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asymmetric assortative mating and queen polyandry are linked to a Supergene controlling ant social organization
Molecular Ecology, 2019Co-Authors: Amaury Avril, Jessica Purcell, Alan Brelsford, Michel ChapuisatAbstract:Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these "social Supergenes" affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a Supergene with alternate haplotypes-Sm and Sp-underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male-mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the Supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.
Mathieu Joron - One of the best experts on this subject based on the ideXlab platform.
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Unravelling the genes forming the wing pattern Supergene in the polymorphic butterfly Heliconius numata
EvoDevo, 2019Co-Authors: Suzanne V Saenko, Mathieu Chouteau, Mathieu Joron, Corinne Blugeon, Florence Piron-prunier, Violaine LlaurensAbstract:Background: Unravelling the genetic basis of polymorphic characters is central to our understanding of the origins and diversification of living organisms. Recently, Supergenes have been implicated in a wide range of complex polymorphisms, from adaptive colouration in butterflies and fish to reproductive strategies in birds and plants. The concept of a Supergene is now a hot topic in biology, and identification of its functional elements is needed to shed light on the evolution of highly divergent adaptive traits. Here, we apply different gene expression analyses to study the Supergene P that controls polymorphism of mimetic wing colour patterns in the neotropical butterfly Heliconius numata. Results: We performed de novo transcriptome assembly and differential expression analyses using high-throughput Illumina RNA sequencing on developing wing discs of different H. numata morphs. Within the P interval, 30 and 17 of the 191 transcripts were expressed differentially in prepupae and day-1 pupae, respectively. Among these is the gene cortex, known to play a role in wing pattern formation in Heliconius and other Lepidoptera. Our in situ hybridization experiments confirmed the relationship between cortex expression and adult wing patterns. Conclusions: This study found the majority of genes in the P interval to be expressed in the developing wing discs during the critical stages of colour pattern formation, and detect drastic changes in expression patterns in multiple genes associated with structural variants. The patterns of expression of cortex only partially recapitulate the variation in adult phenotype, suggesting that the remaining phenotypic variation could be controlled by other genes within the P interval. Although functional studies on cortex are now needed to determine its exact developmental role, our results are in accordance with the classical Supergene hypothesis, whereby several genes inherited together due to tight linkage control a major developmental switch.
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how heterozygote advantage can promote the evolution of disassortative mating and shape the underlying genetic architecture
bioRxiv, 2019Co-Authors: Ludovic Maisonneuve, Mathieu Chouteau, Mathieu Joron, Violaine LlaurensAbstract:Abstract Mate preferences exert strong selection on the evolution of trait variations. Here we aimed at understanding the evolution of disassortative mating based on the emblematic example of polymorphism in mimetic color patterns in the defended butterfly Heliconius numata. Positive frequency-dependent selection is exerted on wing color pattern by predators learning the association between warning coloration and chemical defenses, resulting in selection promoting mimicry toward local communities of defended species. In this well-characterized adaptive landscape, chromosomal inversions in the Supergene controlling wing pattern variations have been reported. These inversions are often associated with deleterious mutations, inducing a heterozygote advantage at the Supergene, favoring the evolution of disassortative mating based on wing color pattern. To explore the conditions underlying the emergence of disassortative mating, we modeled both the color pattern locus and a mate preference locus. We confirm that a heterozygote advantage favor the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one Supergene allele is free from any genetic load. Comparisons of hypothetical genetic architecture underlying mate choice behaviors show that rejection alleles linked to the Supergene can be under positive selection and enable the emergence of disassortative mating behaviour.
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unravelling the genes forming the wing pattern Supergene in the polymorphic butterfly heliconius numata
Evodevo, 2019Co-Authors: Suzanne V Saenko, Mathieu Chouteau, Mathieu Joron, Florence Pironprunier, Corinne Blugeon, Violaine LlaurensAbstract:Unravelling the genetic basis of polymorphic characters is central to our understanding of the origins and diversification of living organisms. Recently, Supergenes have been implicated in a wide range of complex polymorphisms, from adaptive colouration in butterflies and fish to reproductive strategies in birds and plants. The concept of a Supergene is now a hot topic in biology, and identification of its functional elements is needed to shed light on the evolution of highly divergent adaptive traits. Here, we apply different gene expression analyses to study the Supergene P that controls polymorphism of mimetic wing colour patterns in the neotropical butterfly Heliconius numata. We performed de novo transcriptome assembly and differential expression analyses using high-throughput Illumina RNA sequencing on developing wing discs of different H. numata morphs. Within the P interval, 30 and 17 of the 191 transcripts were expressed differentially in prepupae and day-1 pupae, respectively. Among these is the gene cortex, known to play a role in wing pattern formation in Heliconius and other Lepidoptera. Our in situ hybridization experiments confirmed the relationship between cortex expression and adult wing patterns. This study found the majority of genes in the P interval to be expressed in the developing wing discs during the critical stages of colour pattern formation, and detect drastic changes in expression patterns in multiple genes associated with structural variants. The patterns of expression of cortex only partially recapitulate the variation in adult phenotype, suggesting that the remaining phenotypic variation could be controlled by other genes within the P interval. Although functional studies on cortex are now needed to determine its exact developmental role, our results are in accordance with the classical Supergene hypothesis, whereby several genes inherited together due to tight linkage control a major developmental switch.
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Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion
Current Biology, 2018Co-Authors: Annabel Whibley, Lise Frézal, Reuben W. Nowell, James Mallet, Kanchon K. Dasmahapatra, María Ángeles Rodríguez De Cara, Mathieu JoronAbstract:Summary Supergenes are groups of tightly linked loci whose variation is inherited as a single Mendelian locus and are a common genetic architecture for complex traits under balancing selection [1–8]. Supergene alleles are long-range haplotypes with numerous mutations underlying distinct adaptive strategies, often maintained in linkage disequilibrium through the suppression of recombination by chromosomal rearrangements [1, 5, 7–9]. However, the mechanism governing the formation of Supergenes is not well understood and poses the paradox of establishing divergent functional haplotypes in the face of recombination. Here, we show that the formation of the Supergene alleles encoding mimicry polymorphism in the butterfly Heliconius numata is associated with the introgression of a divergent, inverted chromosomal segment. Haplotype divergence and linkage disequilibrium indicate that Supergene alleles, each allowing precise wing-pattern resemblance to distinct butterfly models, originate from over a million years of independent chromosomal evolution in separate lineages. These "superalleles" have evolved from a chromosomal inversion captured by introgression and maintained in balanced polymorphism, triggering Supergene inheritance. This mode of evolution involving the introgression of a chromosomal rearrangement is likely to be a common feature of complex structural polymorphisms associated with the coexistence of distinct adaptive syndromes. This shows that the reticulation of genealogies may have a powerful influence on the evolution of genetic architectures in nature.
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Supergene evolution triggered by the introgression of a chromosomal inversion
bioRxiv, 2017Co-Authors: Annabel Whibley, Lise Frézal, Angeles De Cara, Reuben W. Nowell, James Mallet, Kanchon K. Dasmahapatra, Mathieu JoronAbstract:Supergenes are groups of tightly linked loci whose variation is inherited as a single Mendelian locus and are a common genetic architecture for complex traits under balancing selection. Supergene alleles are long-range haplotypes with numerous mutations underlying distinct adaptive strategies, often maintained in linkage disequilibrium through the suppression of recombination by chromosomal rearrangements. However, the mechanism governing the formation of Supergenes is not well understood, and poses the paradox of establishing divergent functional haplotypes in face of recombination. Here, we show that the formation of the Supergene alleles encoding mimicry polymorphism in the butterfly Heliconius numata is associated with the introgression of a divergent, inverted chromosomal segment. Haplotype divergence and linkage disequilibrium indicate that Supergene alleles, each allowing precise wing-pattern resemblance to distinct butterfly models, originate from over a million years of independent chromosomal evolution in separate lineages. These "superalleles" have evolved from a chromosomal inversion captured by introgression and maintained in balanced polymorphism, triggering Supergene inheritance. This mode of evolution is likely to be a common feature of complex structural polymorphisms associated with the coexistence of distinct adaptive syndromes, and shows that the reticulation of genealogies may have a powerful influence on the evolution of genetic architectures in nature.
Jessica Purcell - One of the best experts on this subject based on the ideXlab platform.
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maternal effect killing by a Supergene controlling ant social organization
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Amaury Avril, Sebastien Beniguel, Jessica Purcell, Michel ChapuisatAbstract:Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the Supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social Supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.
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An Ancient and Eroded Social Supergene Is Widespread across Formica Ants
Current biology : CB, 2020Co-Authors: Alan Brelsford, Amaury Avril, Jessica Purcell, Liselotte Sundström, Heikki Helanterä, Patrick Tran Van, Junxia Zhang, Timothée Brütsch, Michel ChapuisatAbstract:Summary Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [ 1 , 2 ]. Although Supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [ 3 ]. Here, we uncover 20–40 Ma of evolutionary history of a Supergene associated with polymorphic social organization in Formica ants [ 4 ]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the Supergene’s size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative Supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the Supergene. This unexpected pattern of divergence indicates that the Formica Supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [ 5 ]. We propose an alternative “eroded strata model” in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the Supergene contains a transcription factor essential for motor neuron development in Drosophila [ 6 ]. The discovery that a very small portion of this large and ancient Supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.
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asymmetric assortative mating and queen polyandry are linked to a Supergene controlling ant social organization
Molecular Ecology, 2019Co-Authors: Amaury Avril, Jessica Purcell, Alan Brelsford, Michel ChapuisatAbstract:Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these "social Supergenes" affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a Supergene with alternate haplotypes-Sm and Sp-underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male-mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the Supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.
Dewayne Shoemaker - One of the best experts on this subject based on the ideXlab platform.
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unexpected patterns of segregation distortion at a selfish Supergene in the fire ant solenopsis invicta
BMC Genetics, 2018Co-Authors: Kenneth G Ross, Dewayne ShoemakerAbstract:The Sb Supergene in the fire ant Solenopsis invicta determines the form of colony social organization, with colonies whose inhabitants bear the element containing multiple reproductive queens and colonies lacking it containing only a single queen. Several features of this Supergene — including suppressed recombination, presence of deleterious mutations, association with a large centromere, and “green-beard” behavior — suggest that it may be a selfish genetic element that engages in transmission ratio distortion (TRD), defined as significant departures in progeny allele frequencies from Mendelian inheritance ratios. We tested this possibility by surveying segregation ratios in embryo progenies of 101 queens of the “polygyne” social form (3512 embryos) using three Supergene-linked markers and twelve markers outside the Supergene. Significant departures from Mendelian ratios were observed at the Supergene loci in 3–5 times more progenies than expected in the absence of TRD and than found, on average, among non-Supergene loci. Also, Supergene loci displayed the greatest mean deviations from Mendelian ratios among all study loci, although these typically were modest. A surprising feature of the observed inter-progeny variation in TRD was that significant deviations involved not only excesses of Supergene alleles but also similarly frequent excesses of the alternate alleles on the homologous chromosome. As expected given the common occurrence of such “drive reversal” in this system, alleles associated with the Supergene gain no consistent transmission advantage over their alternate alleles at the population level. Finally, we observed low levels of recombination and incomplete gametic disequilibrium across the Supergene, including between adjacent markers within a single inversion. Our data confirm the prediction that the Sb Supergene is a selfish genetic element capable of biasing its own transmission during reproduction, yet counterselection for suppressor loci evidently has produced an evolutionary stalemate in TRD between the variant homologous haplotypes on the “social chromosome”. Evidence implicates prezygotic segregation distortion as responsible for the TRD we document, with “true” meiotic drive the most likely mechanism. Low levels of recombination and incomplete gametic disequilibrium across the Supergene suggest that selection does not preserve a single uniform Supergene haplotype responsible for inducing polygyny.
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Additional file 16: of Unexpected patterns of segregation distortion at a selfish Supergene in the fire ant Solenopsis invicta
2018Co-Authors: Kenneth Ross, Dewayne ShoemakerAbstract:Figure S10. Hypothetical scenario for a historical double crossover involving the putative Supergene drive locus as the genetic mechanism responsible for Sb Supergene drive reversal in polygyne Solenopsis invicta. (A) Double crossover between the wild-type Sb and SB social chromosomes in the segment between markers i_126 and Gp-9 transferred the complete drive complex (locus) from Sb to SB without altering the congruence of alleles at all three Supergene markers observed in progenies with both drive and reversal-of-drive. Two novel recombination products were generated, a SB chromosome containing the drive locus and a Sb chromosome without it, and these presumably must be paired in a queen to yield drive reversal in her progeny (pairing of wild-type SB with wild-type Sb yields Supergene (Sb) drive; pairing leading to any of six different drive-locus+ or drive-locus− homozygotes is expected to yield Mendelian proportions, although at least some of these homozygotes are expected to be lethal genotypes in queens; and pairing leading to either of two drive-locus+/drive locus– heterozygotes on otherwise SB or Sb haplotypes in homozygous condition is expected to yield drive that is undetectable). (B) Sequence differentiation between SB (N = 60) and Sb (N = 20) social chromosomes from native (South American) S. invicta, as measured by differences in the pooled SB nucleotide diversity (π) and the median values of absolute sequence divergence (dxy) between individual chromosomes of each type along 5 kb non-overlapping windows. Values significantly greater than zero (substantially above blue line), consistent with recombination of Sb segments into SB haplotypes, are rare and involve small segments. Asterisks indicate three such instances of likely recombination of ≈5-10 kb-size elements. Positions of the three inversions contained within the Supergene are shown by the blue bars. (C) Linkage disequilibrium (LD, measured as r2 values) in native S. invicta along the SB social chromosome (N = 60). Outside of the centromere, LD is weak, as expected given the lack of sizeable inversions and predicted resultant free recombination. Data for Panels B and C were obtained from whole-genome sequence assemblies (Y. Zheng et al., unpublished; [104]). Centromere is not shown to scale in any of the figures. (TIF 1.53 mb
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male reproductive fitness and queen polyandry are linked to variation in the Supergene gp 9 in the fire ant solenopsis invicta
Proceedings of The Royal Society B: Biological Sciences, 2012Co-Authors: Lucinda P Lawson, Robert Vander K Meer, Dewayne ShoemakerAbstract:Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in Supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic Supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9b males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9b males remain highly receptive to remating. Queens mated to multiple Gp-9B males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9b males have significantly lower sperm counts than Gp-9B males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9b males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9b allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9b allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.
