Origin and Evolution of the Dependent Lineages in the Genetic Caste Determination System of Pogonomyrmex Ants

Sirviö, Anu; Pamilo, Pekka; Johnson, Robert A.; Page, Robert E.; Gadau, Juergen

doi:10.1111/j.1558-5646.2010.01170.x

Cited by 37 publications

(51 citation statements)

References 45 publications

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“…Introgression through rare hybrid queen production may therefore remain undetected while using only a handful of marker loci. Rare development of queens from hybrid eggs has been reported in other ant systems relying on hybridization between divergent lineages [18,[44][45][46]. Though, not a single C. hispanica hybrid queen has been found so far ( [9]; this study).…”

Section: Discussionmentioning

confidence: 75%

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Large-scale distribution of hybridogenetic lineages in a Spanish desert ant

2014

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Recently, a unique case of hybridogenesis at a social level was reported in local populations of the desert ants Cataglyphis. Queens mate with males originating from a different genetic lineage than their own to produce hybrid workers, but they use parthenogenesis for the production of reproductive offspring (males and females). As a result, non-reproductive workers are all inter-lineage hybrids, whereas the sexual line is purely maternal. Here, we show that this unorthodox reproductive system occurs in all populations of the ant Cataglyphis hispanica. Remarkably, workers are hybrids of the same two genetic lineages along a 400 km transect crossing the whole distribution range of the species. These results indicate that social hybridogenesis in C. hispanica allows their maintenance over time and across a large geographical scale of two highly divergent genetic lineages, despite their constant hybridization. The widespread distribution of social hybridogenesis in C. hispanica supports that this reproductive strategy has been evolutionarily conserved over a long period.

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Section: Discussionmentioning

confidence: 75%

“…Though, not a single C. hispanica hybrid queen has been found so far ( [9]; this study). Future linkage studies using a larger number of nuclear makers [46] will help to determine whether His1/ His2 have achieved complete genetic isolation or whether some parts of their genome are leaky.…”

Section: Discussionmentioning

confidence: 99%

Large-scale distribution of hybridogenetic lineages in a Spanish desert ant

2014

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“…Nevertheless, interlineage hybrid queens of Pogonomyrmex are known to have reduced fitness, if any [17]. Accordingly, analyses of both nuclear and mtDNA have failed to provide any evidence of gene flow among lineages [19]. (iii) Alternatively, the introgression of mtDNA among lineages may stem from gynogenesis, which is an incomplete form of parthenogenesis whereby a sperm cell comes into contact with the egg, but does not transmit its nucleus to the zygote [20].…”

Section: Discussionmentioning

confidence: 99%

Introgression of mitochondrial DNA among lineages in a hybridogenetic ant

Darras

Aron

2015

Biol. Lett.

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We report a remarkable pattern of incongruence between nuclear and mitochondrial variations in a social insect, the desert ant Cataglyphis hispanica. This species reproduces by social hybridogenesis. In all populations, two distinct genetic lineages coexist; non-reproductive workers develop from hybrid crosses between the lineages, whereas reproductive offspring (males and new queens) are typically produced asexually by parthenogenesis. Genetic analyses based on nuclear markers revealed that the two lineages remain highly differentiated despite constant hybridization for worker production. Here, we show that, in contrast with nuclear DNA, mitochondrial DNA (mtDNA) does not recover the two lineages as monophyletic. Rather, mitochondrial haplotypes cluster according to their geographical origin. We argue that this cytonuclear incongruence stems from introgression of mtDNA among lineages, and review the mechanisms likely to explain this pattern under social hybridogenesis.

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“…For each species, we estimated the median gene GC content of orthologs in a given GO group and subtracted from this the median gene GC for all genes in that species and standardized this difference by dividing by the median absolute deviation of GC content for that species, creating the nonparametric equivalent of a z-score. All four species have known recombination rates (9,10,(54)(55)(56) [note: P. barbatus is part of the barbatus/rugosus complex and hybrids occur between species; we used the recombination rate determined for Pogonomyrmex rugosus (56) to approximate the P. barbatus rate]. The effect of recombination rate on GC content was examined with GO group as a random factor using Restricted Maximum Likelihood (REML) with the R function lmer, and significance was determined by comparing twice the difference in maximum likelihoods of the reduced and full model to a χ 2 with one degree of freedom.…”

Section: Analysis Of Gc Content and Recombination Across Four Hymenopmentioning

confidence: 99%

Recombination is associated with the evolution of genome structure and worker behavior in honey bees

Kent

Minaei

Harpur

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The rise of insect societies, marked by the formation of reproductive and sterile castes, represents a major unsolved mystery in evolution. Across several independent origins of sociality, the genomes of social hymenopterans share two peculiar attributes: high recombination and low but heterogeneous GC content. For example, the genome of the honey bee, Apis mellifera, represents a mosaic of GC-poor and GC-rich regions with rates of recombination an order of magnitude higher than in humans. However, it is unclear how heterogeneity in GC content arises, and how it relates to the expression and evolution of worker traits. Using population genetic analyses, we demonstrate a bias in the allele frequency and fixation rate of derived C or G mutations in high-recombination regions, consistent with recombination's causal influence on GCcontent evolution via biased gene conversion. We also show that recombination and biased gene conversion actively maintain the heterogeneous GC content of the honey bee genome despite an overall A/T mutation bias. Further, we found that GC-rich genes and intergenic regions have higher levels of genetic diversity and divergence relative to GC-poor regions, also consistent with recombination's causal influence on the rate of molecular evolution. Finally, we found that genes associated with behavior and those with worker-biased expression are found in GC-rich regions of the bee genome and also experience high rates of molecular evolution. Taken together, these findings suggest that recombination acts to maintain a genetically diverse and dynamic part of the genome where genes underlying worker behavior evolve more quickly. E usociality, characterized by reproductive division of labor and cooperative brood care, independently evolved multiple times in insects (1). The causes for this major evolutionary transition have been intensely debated (2, 3). Although kin-selection theory provides a general mechanism whereby altruistic and cooperative behaviors can evolve (4), we still lack an understanding of how the genomes of social organisms modulate the expression and evolution of phenotypically distinct castes. Previous studies have uncovered two unusual properties of social hymenopteran genomes. Eusocial hymenoptera have the highest recombination rates of any group in the Animalia (5-7), and the honey bee, Apis mellifera, has the highest recombination rate recorded in higher eukaryotes (19 cM/Mb) (8-10). Eusocial hymenoptera also have low but heterogeneous GC content (11-13). Moreover, the honey bee genome exhibits a remarkable degree of heterogeneity in recombination rates (10) and GC content (12, 13), and the two show a great deal of covariance (10).We find the association between the evolution of eusociality and the evolution of high recombination rates intriguing because recombination has a well-established causal effect on GC-content evolution (14-20), the rate of molecular evolution (18,21,22), and the efficiency of natural selection (23-28). Recombination affects GC-content evolution in euk...

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Origin and Evolution of the Dependent Lineages in the Genetic Caste Determination System of Pogonomyrmex Ants

Cited by 37 publications

References 45 publications

Large-scale distribution of hybridogenetic lineages in a Spanish desert ant

Large-scale distribution of hybridogenetic lineages in a Spanish desert ant

Introgression of mitochondrial DNA among lineages in a hybridogenetic ant

Recombination is associated with the evolution of genome structure and worker behavior in honey bees

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