Adaptive, caste-specific changes to recombination rates in a thelytokous honeybee population

Abstract

The ability to clone oneself has clear benefits—no need for mate hunting or dilution of one's genome in offspring. It is therefore unsurprising that some populations of haplo-diploid social insects have evolved thelytokous parthenogenesis—the virgin birth of a female. But thelytokous parthenogenesis has a downside: the loss of heterozygosity (LoH) as a consequence of genetic recombination. LoH in haplo-diploid insects can be highly deleterious because female sex determination often relies on heterozygosity at sex-determining loci. The two female castes of the Cape honeybee, Apis mellifera capensis , differ in their mode of reproduction. While workers always reproduce thelytokously, queens always mate and reproduce sexually. For workers, it is important to reduce the frequency of recombination so as to not produce offspring that are homozygous. Here, we ask whether recombination rates differ between Cape workers and Cape queens that we experimentally manipulated to reproduce thelytokously. We tested our hypothesis that Cape workers have evolved mechanisms that restrain genetic recombination, whereas queens have no need for such mechanisms because they reproduce sexually. Using a combination of microsatellite genotyping and whole-genome sequencing we find that a reduction in recombination is confined to workers only.

Co-segregation of recombinant chromatids maintains genome-wide heterozygosity in an asexual nematode

“…We suggest that DCA may exist in other asexuals displaying highly heterozygous genomes. For instance, DCA is compatible with the absence or very reduced LOH found in the recombining parthenogenetic water flea Daphnia magna ( 25 ), the asexual females produced by Cape Honey Bee workers ( 26 ) or the Rotifer Adineta vaga ( 9 ).…”

“…We discovered DCA, as a new mechanism of LOH avoidance despite recombination. Another mechanism of LOH avoidance have been previously proposed for recombining asexuals, which relies on distal crossing-over location ( 6, 26 ). However, distal crossing-overs are very unstable for the C. elegans holocentric chromosomes and often lead to aneuploidy ( 27 ), suggesting that such mechanism of LOH avoidance could not have been selected in a holocentric species such as M. belari .…”

Cosegregation of recombinant chromatids maintains genome-wide heterozygosity in an asexual nematode

“…Another mechanism of LOH avoidance has been previously proposed for recombining asexuals, which relies on distal crossover location ( 6 , 30 ). However, distal crossovers are very unstable for the C. elegans holocentric chromosomes and often lead to aneuploidy ( 31 ), suggesting that such mechanism of LOH avoidance could not have been selected in a holocentric species such as M. belari .…”

“…In most cases, the level of recombination in the asexual lineages was inferred from the observed rate of LOH. For the Cape honey bee, the crustaceans Artemia parthenogenetica and Daphnia magna or the ant Cerapachys biroi to only cite a few, a reduction in the rate of recombination has been invoked to account for the observed level of elevated heterozygosity and absence of LOH ( 6 , 30 , 38 , 39 ). In the light of our discovery in M. belari , we would like to propose CRC as a possible alternative explanation.…”

On the utility of oddities: exceptional bee reproduction illuminates fundamental questions of recombination

“…Leveraging the remarkable genetics of the cape honeybee Apis mellifera capensis, a new paper in the Proceedings of the Royal Society B reports a remarkable case of modulation of recombination in a single species [9]. While A. m. capensis colony structure shares much with other honeybees, with a dominant queen who mates with many males to produce a genetically diverse colony, A. m. capensis workers are unique in regularly laying diploid femaleproducing eggs.…”