Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta

Keller, Laurent; Ross, Mark

doi:10.1046/j.1420-9101.1999.00064.x

Cited by 55 publications

(84 citation statements)

References 42 publications

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“…It is at this point that selection acts in the queen caste. Under the superlocus framework, only the queens with the superlocus genotypes S 1 S 3 and S 2 S 3 survive to reproduce (Ross 1997;Keller and Ross 1999). The surviving queens then produce the next generation of prereproductive queens, males, and workers, which comprise the three castes in this species.…”

Section: Expected Patterns Of Genetic Variationmentioning

confidence: 99%

“…This study was motivated by previous work in polygyne S. invicta that attempted to explain patterns of genetic variation at the loci Pgm-3 and Gp-9 (Ross 1992(Ross , 1997Ross and Shoemaker 1993;Ross and Keller 1995;Keller and Ross 1999). The most recent investigations suggested that variation at these loci was influenced by selection acting on Gp-9 in combination with gene flow via conspecific monogyne males.…”

Section: Selection Gene Flow and Genotypic Structure Of Polygyne Somentioning

confidence: 99%

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A Formal Assessment of Gene Flow and Selection in the Fire Ant Solenopsis Invicta

2000

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Abstract. Recent studies of the introduced fire ant Solenopsis invicta suggest that introduced polygyne (with multiple queens per nest) populations are strongly influenced by male-mediated gene flow from neighboring monogyne (single queen per nest) populations and selection acting on a single locus, general . This investigation formally tests this hypothesis and determines if these processes can account for the genotypic structure of polygyne S. invicta. To increase the statistical power of this test, we considered the genotypes of polygyne queens and workers at both Gp-9 and the closely linked, selectively neutral locus Pgm-3. We then constructed and analyzed a novel mathematical model to delimit the effects of monogyne male gene flow and selection on the joint genotypes at the Pgm-3/Gp-9 superlocus. Using this framework, a hierarchical maximum-likelihood method was developed to estimate the bestfitting gene flow and selection parameters based on the fit of our model to data from both the current study and an earlier one of the same population. In each case, selection on polygyne queens and workers alone, with no monogyne male gene flow, provides the most parsimonious explanation for the observed genotype frequencies. The apparent discrepancy between this result and the empirical evidence for monogyne male gene flow indicates that undocumented factors, such as other forms of selection in polygyne males or workers, are operating in introduced polygyne S. invicta.Key words. Fire ants, gene flow, isozymes, migration-selection balance, population structure, selection, Solenopsis invicta.Received March 2, 1999. Accepted September 1, 1999.Gene flow and selection are fundamental evolutionary processes that may act jointly to shape patterns of genetic variation within populations. For example, selection against deleterious alleles may reduce variation, whereas gene flow from nearby populations may act in opposition to such selection by reintroducing unfit alleles (May et al. 1975;Felsenstein 1976;Endler 1977;Barton and Hewitt 1985;Slatkin 1985;Barton and Clark 1990). Several studies have reported such a migration-selection balance within species (McNeilly 1968;Livingstone 1969;Jones et al. 1977;Turner 1977;Jones 1982;Riechert 1993;King and Lawson 1995;Chevillon et al. 1998). One well-studied case is found in introduced populations of the fire ant Solenopsis invicta in the United States, where it was thought that a recessive deleterious allele at the locus phosphoglucomutase-3 (Pgm-3) was maintained at high frequency in one social form by gene flow from neighboring populations of the alternate social form (Ross 1992;Ross and Shoemaker 1993;Ross and Keller 1995).The role of Pgm-3, however, was recently challenged by the discovery of the diallelic locus general protein-9 (Gp-9), which is tightly linked (r ϭ 0.0016) to Pgm-3 and apparently under strong selection in S. invicta. In monogyne (with a single queen per nest) populations, all females are genotype Gp-9 BB , and so the monogyne form is fixed for the Gp-9 B allele. ...

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Section: Expected Patterns Of Genetic Variationmentioning

confidence: 99%

Section: Selection Gene Flow and Genotypic Structure Of Polygyne Somentioning

confidence: 99%

A Formal Assessment of Gene Flow and Selection in the Fire Ant Solenopsis Invicta

2000

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“…The monogyne and polygyne social forms differ in numerous important aspects of their biology, including the level of aggression between colonies and how new colonies are initiated 9 . These important behavioural differences are associated with a suite of morphological and life-history differences among individuals with alternative Gp-9 genotypes, including queen fecundity, their tendency to accumulate fat during sexual maturation, the odour of mature queens, the number of sperm produced by males, and the size of workers [4][5][6][7][10][11][12] . The fact that Gp-9 codes for an odorant-binding protein (OBP), coupled with evidence that selection acted to drive the molecular divergence of Gp-9b alleles from the ancestral Gp-9B allele, has led to the suggestion that this gene may have a direct role in regulating social organization by means of chemical communication 7,13 .…”

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confidence: 99%

“…The fact that Gp-9 codes for an odorant-binding protein (OBP), coupled with evidence that selection acted to drive the molecular divergence of Gp-9b alleles from the ancestral Gp-9B allele, has led to the suggestion that this gene may have a direct role in regulating social organization by means of chemical communication 7,13 . However, because it is unlikely that an OBP also affects traits as diverse as female size, female fecundity and male spermatogenesis, it has been suggested that Gp-9 might be part of a supergene comprising many genes in tight linkage 10,12,14 . The existence of such clusters of loci facilitating the co-segregation of adaptive variation has been demonstrated in some classical cases of floral types (for example, ref.…”

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A Y-like social chromosome causes alternative colony organization in fire ants

Wang

Wurm

Nipitwattanaphon

et al. 2013

Nature

383

520

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Intraspecific variability in social organization is common, yet the underlying causes are rarely known [1][2][3] . In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene [4][5][6][7][8] . Here we characterize the genomic region responsible for this important social polymorphism, and show that it is part of a pair of heteromorphic chromosomes that have many of the key properties of sex chromosomes. The two variants, hereafter referred to as the social B and social b (SB and Sb) chromosomes, are characterized by a large region of approximately 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromosomes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differentiation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations, including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between individuals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.The fire ant S. invicta is characterized by a remarkable form of social polymorphism under the control of a single Mendelian factor [4][5][6]8 . Remarkably, a genomic element marked by the gene Gp-9 determines whether workers tolerate a single fertile queen (monogyne social form) or several fertile queens (polygyne social form) in their colony. Colonies containing only homozygous Gp-9BB workers accept only a single Gp-9BB queen, whereas colonies containing both Gp-9BB and Gp-9Bb workers will invariably accept several queens, but only Gp-9Bb queens 7,8 . The monogyne and polygyne social forms differ in numerous important aspects of their biology, including the level of aggression between colonies and how new colonies are initiated 9 . These important behavioural differences are associated with a suite of morphological and life-history differences among individuals with alternative Gp-9 genotypes, including queen fecundity, their tendency to accumulate fat during sexual maturation, the odour of mature queens, the number of sperm produced by males, and the size of workers [4][5][6][7][10][11][12] . The fact that Gp-9 codes for an odorant-binding protein (OBP), coupled with evidence that selection acted to drive the molecular diverg...

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To b or not to b: A pheromone-binding protein regulates colony social organization in fire ants

Krieger

2004

Bioessays

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A major distinction in the social organization of ant societies is the number of reproductive queens that reside in a single colony. The fire ant Solenopsis invicta exists in two distinct social forms, one with colonies headed by a single reproductive queen and the other containing several to hundreds of egg-laying queens. This variation in social organization has been shown to be associated with genotypes at the gene Gp-9. Specifically, single-queen colonies have only the B allelic variant of this gene, whereas multiple-queen colonies always have the b variant as well. Subsequent studies revealed that Gp-9 shares the highest sequence similarity with genes encoding pheromone-binding proteins (PBPs). In other insects, PBPs serve as central molecular components in the process of chemical recognition of conspecifics. Fire ant workers regulate the number of egg-laying queens in a colony by accepting queens that produce appropriate chemical signals and destroying those that do not. The likely role of GP-9 in chemoreception suggests that the essential distinction in colony queen number between the single and multiple-queen form originates from differences in workers' abilities to recognize queens. Other, closely related fire ant species seem to regulate colony social organization in a similar fashion.

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Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta

Cited by 55 publications

References 42 publications

A Formal Assessment of Gene Flow and Selection in the Fire Ant Solenopsis Invicta

A Formal Assessment of Gene Flow and Selection in the Fire Ant Solenopsis Invicta

A Y-like social chromosome causes alternative colony organization in fire ants

To b or not to b: A pheromone-binding protein regulates colony social organization in fire ants

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