Ross lab roadmap

History of fire ant (Solenopsis invicta) research by Ross lab and collaborators.

Summary slides © Dr. Kenneth Ross

roadmap1

roadmap2

Ross and Fletcher (1985): Use allozyme at two loci for genetic structure. Foundress M queens singly inseminated. Average relatedness among female nestmates of M is 0.714, ~not different from 0.75. P queens also singly inseminated, not more related to nestmate queens then to other queens. No evidence of sub-population or inbreeding in P colonies.

“These results do not support the view that kin selection has promoted the evolution of polygyny in North American S. invicta. Rather, mutualism appears to be the most likely selective factor mediating queen associations in this ant”

Ross (1988): Use genetic markers to assess maternity in P queens. Some queens in P colony produce much more sexuals. But such queens would lose weight and die soon, won’t last long.

Ross (1992) American Naturalist: Breeding system review. Queens only mate once. Very low relatedness among nest-mate P queens. Variance in maternity among queens or inter-nest movement of ants as determinants of colony genetic structure.

Ross, Vargo, Keller and Trager (1993): More diploid males in introduced population than native pop., excluded mating times and level of inbreeding, so concluded that the higher % diploid is because of loss of sex-determining loci allele diversity, (from founder event)

Keller (1993): Suggests reproductive success of queens in polygyne colonies cannot be considered only with # of offspring they produce, but also

Keller and Ross (1993, 1995): G (genotype) x E (queen #) interaction

Pgm-3 genotype frequency, Pgm-3 genotype (aa) correlate with heavier queen weight (reproductive fitness) in P. (ab) also > (bb) in weight. Effect of queen number: queens reared in colony fragment made M were heavier than those in P fragment, → pheromone level reproductive affects development, but not the key factor, genotype also matters.

Ross and Keller (1995) American Naturalist: review on social structure.

Shoemaker and Ross (1996) Nature: Allozyme, strong structure nest level, both M and P. Microsatellites: weak structure above nest level in P only. mtDNA: diff at this level in P only too.

Ross, Vargo and Keller (1996): introduced vs. native populations of fire ants, social evolution: diff in number of queens, relatedness, greater % of permanently unmated queens; loss of alleles at sex locus, skew of sex ratio.

Keller and Ross (1998) Nature: Worker discrimination towards BB queens: BB queens initiating reproduction are killed by Bb workers. Indicates Gp-9 linked to a green-bread allele. Workers appear to distinguish BB from Bb queens on the basis of a transferable odor cue.

Ross and Keller (1998) PNAS:   Confirms queen weight influenced by Gp-9, BB queen significantly heavier than Bb. Young queen, however, weight the same. Assay on P workers response to different queens: all M queens are destroyed, also polygyne queen with BB genotype.

DeHeer, Goodisman and Ross (1999): Queen dispersal: BB – most agility go away to open land, Bb – mixed strategy, but tend to re-enter, bb – lack energy reserve for mating flight, not viable

Goodisman et al. (1999): Correlation between Gp-9 genotype and worker mass, BB>Bb>bb

Goodisman, Ross and Asmussen (2000): selection on P queens and workers along, without M male gene flow, give the most parsimonious explanation for genotype frequencies in nature. — test if Gp-9 is the main gen; test how much gene flow by M males.

Krieger and Ross (2002) Science: sequenced Gp-9, found it encodes a OBP. phylogenetic relationship of Gp-9 alleles in 10 Solenopsis species, found Gp-9 conserved in South American fire ants with social polymorphism, suggest positive selection on alleles for diff social forms.

Gotzek and Ross (2008): convert queenright M colonies to Polygyne by adding broods.

“we addressed this problem by fostering polygyne brood into queenright monogyne colonies. All such treatment colonies switched social organization to become polygyne, coincident with their proportions of b-bearing workers exceeding 12%. “

Gotzek and Ross (2009): a review on the fire ants model system

Eliyahu et al. (2011): chemical analysis of cuticular components:  venom alkaloids (the most abundnat component) differ between queens and workers, also between reproductive or not. M vs. P workers differ in alkaloid composition. Mature non-reproductive P queens higher in % of cis-piperidine alkaloids than less reproductive queens, also BB queen higher piperidine than Bb queen. The most abundant one is c11-piperidine, which is absent in workers. In CHC, higher alkenes/alkadienes in reproductive queen with b allele (than non-reproductive or BB queen).

“We found that the composition of the most abundant components, venom alkaloids, differed between queens and workers, as well as between reproductive and non-reproductive queens. Additionally, workers of the two forms could be distinguished by alkaloid composition. Finally, sexually mature, non-reproductive queens from polygyne colonies differed in their proportions of cis-piperidine alkaloids, depending on their Gp-9 genotype, although the difference disappeared once they became functional reproductives. Among the unsaturated cuticular hydrocarbons characteristic of queens, there were differences in amounts of alkenes/alkadienes between non-reproductive polygyne queens of different Gp-9 genotypes, between non-reproductive and reproductive queens, and between polygyne and monogyne reproductive queens, with the amounts increasing at a relatively higher rate through reproductive ontogeny in queens bearing the Gp-9 b allele.”

Lawson, Vander Meer and Showmaker (2012): show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Queens mated with Gp-9b males would likely mate again, to get Gp-9B. Queens mated with Gp-9B rarely mate again.Gp-9b males have lower sperm counts than Gp-9B males.

“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. 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.”

Nipitwattanaphon et al. (2013): gene expression of queens of diff reprodutive status and of genotype. Viral genes and transposons are more highly expressed in b queens. Candidate chem signaling genes: desaturase, elongase, dehydrogenase, p450, fatty acid synthase & reductase, OBP genes, CSP gene.

Wang et al. (2013): social chromosome with 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. 616 genes.

Huang & Wang (2014): a synthetic review on supergene of fire ants

Trible & Ross (2016). Behavioral evidence of cuticular chemical signals on polygyne queens conveying supergene genotype.

Ross & Shoemaker (2018). Evidence of segregation distortion of Sb supergene

“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.”

Pitts et al. (2018). Revision of the fire ants of the Solenopsis saevissima species-group (Hymenoptera: Formicidae).

Arsenault et al. (2020). Supergene‐mediated gene expression profile

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Dr. Ken Ross collecting fire ants @ Athens, GA,USA 2018

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