A caste differentiation mutant elucidates the evolution of socially parasitic ants

Trible, Waring; Chandra, Vikram; Lacy, Kip D.; Limón, Gina; McKenzie, Sean K.; Olivos-Cisneros, Leonora; Arsenault, Samuel V.; Kronauer, Daniel J. C.

doi:10.1016/j.cub.2023.01.067

Cited by 9 publications

(5 citation statements)

References 78 publications

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“…The recent discovery of a queen-like mutant lineage of O. biroi highlighted such within-species variation in caste phenotypes, and revealed candidate molecular mechanisms for caste evolution in Ooceraea (see Trible et al 2023 ). Comparative genomic studies across and within Ooceraea species with diverse reproductive biology might help identify mechanisms of caste evolution in ants.…”

Section: Discussionmentioning

confidence: 99%

Ooceraea hainingensis sp. nov.: A new Chinese Ooceraea (Hymenoptera, Formicidae, Dorylinae) species with a dealate queen, closely allied to the queenless clonal raider ant O. biroi

Gao,

Long,

Liu

et al. 2024

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The clonal raider ant, Ooceraea biroi, is a queenless species that reproduces asexually, and these traits make it an attractive model system for laboratory research. However, it is unclear where on the ant phylogeny these traits evolved, partly because few closely related species have been described and studied. Here, we describe a new raider ant species, Ooceraea hainingensissp. nov., from Zhejiang, China. This species is closely related to O. biroi but can be distinguished by the following features: 1) workers of O. hainingensissp. nov. have an obvious promesonotal suture and a metanotal groove, whereas these characters are ambiguous in O. biroi; and 2) the subpetiolar process of O. hainingensis is prominent and anteroventrally directed like a thumb with sublinear posteroventral margin, while in O. biroi, it is anteroventrally directed but slightly backward-bent. Molecular phylogenetic analyses confirm that O. hainingensis is genetically distinct from O. biroi. Importantly, unlike O. biroi, O. hainingensis has a queen caste with wings and well-developed eyes. This suggests that the loss of the queen caste and transition to asexual reproduction by workers is specific to O. biroi and occurred after that species diverged from closely related congeneric species.

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Section: Discussionmentioning

confidence: 99%

Ooceraea hainingensis sp. nov.: A new Chinese Ooceraea (Hymenoptera, Formicidae, Dorylinae) species with a dealate queen, closely allied to the queenless clonal raider ant O. biroi

Gao,

Long,

Liu

et al. 2024

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“…Apart from O. biroi, very few collections of Ooceraea are recorded in the literature, meaning that we know almost nothing about within-species variation in reproductive strategies. The recent discovery of a queen-like mutant lineage of O. biroi highlighted such within-species variation in caste phenotypes, and re-ZooKeys 1205: 101-113 (2024), DOI: 10.3897/zookeys.1205.118358 Qionghua Gao et al: A new species of Ooceraea (Hymenoptera, Formicidae, Dorylinae) from China vealed candidate molecular mechanisms for caste evolution in Ooceraea (see Trible et al 2023). Comparative genomic studies across and within Ooceraea species with diverse reproductive biology might help identify mechanisms of caste evolution in ants.…”

Section: Discussionmentioning

confidence: 99%

Figure 1 from: Gao Q, Long J, Liu C, Liu H, Ran H, Lacy KD, Kronauer DJC (2024) Ooceraea hainingensis sp. nov.: A new Chinese Ooceraea (Hymenoptera, Formicidae, Dorylinae) species with a dealate queen, closely allied to the queenless clonal raider ant O. biroi. ZooKeys 1205: 101-113. https://doi.org/10.3897/zookeys.1205.118358

Gao,

Long,

Liu

et al. 2024

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“…We detected crossovers in all known-pedigree pairs, with an average of 2.38 crossovers per meiosis (Figure 3 and Supplementary Table 5; 31 crossovers sampled across the 13 meioses from known-pedigree pairs). Crossovers were distributed across all chromosomes except for the heteromorphic chromosome 13, for which pervasive structural variation severely limits crossover detection 21 . Adjusted for underestimation due to incomplete phasing and non-detection of uninherited crossovers (see Methods), these data suggest that, on average, 5.5 crossovers occur in each meiosis (0.4 crossovers per chromosome, 95% CI 0.3-0.49).…”

Section: Crossovers Occur Every Meiosis Without Loss Of Heterozygositymentioning

confidence: 99%

Unselfish meiotic drive maintains heterozygosity in a parthenogenetic ant

Lacy,

Hart,

Kronauer

2024

Preprint

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According to Mendel′s second law, chromosomes segregate randomly in meiosis. Non-random segregation is primarily known for cases of selfish meiotic drive in females, in which particular alleles bias their own transmission into the oocyte1,2. Here, we report a rare example of unselfish meiotic drive for crossover inheritance in the clonal raider ant,Ooceraea biroi. This species produces diploid offspring parthenogenetically via fusion of two haploid nuclei from the same meiosis3. This process should cause rapid genotypic degeneration due to loss of heterozygosity, which results if crossover recombination is followed by random (Mendelian) segregation of chromosomes4,5. However, by comparing whole genomes of mothers and daughters, we show that loss of heterozygosity is exceedingly rare, raising the possibility that crossovers are infrequent or absent inO. biroimeiosis. Using a combination of cytology and whole genome sequencing, we show that crossover recombination is, in fact, common, but that loss of heterozygosity is avoided because crossover products are faithfully co-inherited. This results from a programmed violation of Mendel′s law of segregation, such that crossover products segregate together rather than randomly. This discovery highlights an extreme example of cellular ″memory″ of crossovers, which could be a common yet cryptic feature of chromosomal segregation.

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A caste differentiation mutant elucidates the evolution of socially parasitic ants

Cited by 9 publications

References 78 publications

Ooceraea hainingensis sp. nov.: A new Chinese Ooceraea (Hymenoptera, Formicidae, Dorylinae) species with a dealate queen, closely allied to the queenless clonal raider ant O. biroi

Ooceraea hainingensis sp. nov.: A new Chinese Ooceraea (Hymenoptera, Formicidae, Dorylinae) species with a dealate queen, closely allied to the queenless clonal raider ant O. biroi

Unselfish meiotic drive maintains heterozygosity in a parthenogenetic ant

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