I’m happy to share a new preprint on the breeding systems of fire ants >>> https://www.authorea.com/users/903412/articles/1278388-reproductive-competition-in-multiple-queen-fire-ant-colonies-insights-from-analyses-of-breeding-systems

Understanding social group formation and structure is vital for understanding social evolution. The number of breeding individuals (breeders), their relatedness, and how reproduction is shared among the breeders comprise the “breeding system” of a species. 

This project started as Kip’s master thesis, where we set up five and eight queen polygyne colony fragments in a long term rearing experiment and genotyped a whole lot of worker and gyne pupae produced by these queens. The goal was to fully characterize the breeding system attributes of fire ants.

Materials and Methods 

• The primary data comes from our long-term laboratory study of breeders and their female progeny in ten polygyne S. invicta colonies collected in northern Georgia 
• Genomic DNA was extracted, and microsatellite genotyping was performed on female progeny, most queens, and their mates 
• Genetic data from earlier studies, including allozyme and microsatellite genotypes from various populations, were reanalyzed 
• Huang et al. (2014) method of moments estimator was chosen for all relatedness estimates because of its consistently low bias and sampling variance in the simulations and its accuracy in test groups of known pedigree relatedness 

Highlighted Results 

• Monogyne colonies have a single queen that mates with one unrelated male, while polygyne colonies have multiple unrelated queens, some mating multiply 
• Queen number varies greatly in polygyne nests, ranging from two to several hundred, and is dynamic over time 
• Daughters in monogyne nests are full sisters (r=0.73), whereas female progeny relatedness in polygyne S. invicta is low between and high within matrilines .
• Polyandry is uncommon, with most queens mating with a single male; however, polyandrous queens tend to be heavier and more fecund 
• Polyandrous queens in our GA-2023 dataset did not differ from monandrous nestmate queens in their relative production of worker or gyne offspring 
• Increased reproductive skew raises average progeny nestmate relatedness, with both maternity and paternity skew prominent in polygyne form 

Reproductive Skew 

• Significant maternity skew was found in laboratory colonies, with M-index (skew index) values higher for gyne than worker offspring .
• Paternity skew was conspicuous in polyandrous queens, with M-index paternity skew values for gyne offspring consistently exceeding those for worker offspring .
• Sb fathers almost always produced fewer offspring than SB fathers, a fact evident in both embryos and pupae from the two Georgia datasets .

Breeder Relatedness 

• Relatedness is negligible between breeders in monogyne colonies .
• Newly produced genotypic data revealed average pairwise relatedness of zero between nestmate queens in polygyne colonies .
• None of the estimates for relatedness components in polygyne S. invicta is significantly greater than zero .

Progeny Relatedness 

• Low estimates (rp(w)=0.086 and rp(g)=0.103) of nestmate progeny relatedness in the wild reflect the moderate to high numbers of nestmate queens in that study and the low relatedness within and between all classes of nestmate breeders .
• In conjunction with low nestmate queen (and mate) relatedness, the rarity of polyandry and strong paternity skew mean that the disparity in relatedness of workers in the same vs. different matrilines is about as large as possible, setting the stage for the emergence of strong genetic conflict between cohabiting queens and between progeny workers in different matrilines .
• The sterile workers do not manipulate care of the brood in any way to enhance average relatedness between the sexual brood and them and that genetic factors or maternal effects do not influence caste determination in S. invicta 

Discussion 

• The Sb haplotype disrupts mating dynamics, amplifies paternity skew, and alters maternal contributions to sexual daughter production .
• Future work should explore how reproductive competition and conflict are resolved in multiple-breeder societies and how this affects evolutionary dynamics when social polymorphisms are under strong genetic regulation .