Thelytokous reproduction and its long-term genomic consequences

• Applicant: Dr. Eckart Stolle
• Subject Area: Evolution, Anthropology
• Term: since 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 445756277

Thelytokous reproduction in animals, a form of parthenogenesis in which female offspring is produced asexual (but not clonal) from unfertilized eggs, occurs in numerous very successful species, such as planarians, aphids, ants, bees and wasps. Even though diploidy is restored, thelytoky is predicted to increase homozygosity because with a certain probability the entire region between a meiotic crossover and end of the chromosome experiences a loss of heterozygosity (LOH). Such a broad LOH is thought to reduce fitness due to the loss of complementation (unmasking of recessive deleterious alleles) and reduction in genetic diversity. Nevertheless, many permanently thelytokous populations or species thrive and are potent invaders, such as globally invasive ants and a parasitic honeybee lineage. They have, unexpectedly, retained their heterozygosity by suppressed recombination or selection against homozygosity at overdominant loci. However, previous studies were controverse and inconclusive due to a lack power and incomprehensive experimental design. To determine the mechanisms the thelytokous animals retain can their heterozygosity (recombination, selection), to determine which genomic regions of the genome are affected or unaffected (i.e. which loci block LOH and how) and how LOH accumulates over short evolutionary time scales, and to understand how thelytoky is evolutionary and geographically stable, we take advantage of an ideal model system, the Cape Honeybee Apis mellifera capensis. The Cape Honeybee is the best studied thelytokous animal and indeed represents an ideal system since it is polymorphic, i.e. some workers produce females (thelytoky), some workers produce haploid males (arrhenotoky), mated queens produce females sexually (and males by arrhenotoky), and there exists a permanently thelytokous, parasitic lineage. As a haplo-diploid, we can take advantage of haploid males for genomics analyses and straight forward recombination mapping. In addition, we recently identified the major thelytoky-regulating locus in the Cape Honeybee, a heterozygous protein-coding gene within a 3-gene-linkage group which shows strong differential expression between thelytokous and arrhenotokous individuals. We thus can use this thelytoky locus as a positive control and marker for differential gene expression, for the mode of parthenogenesis, and together with the obligate heterozygous sex locus, for loci blocking further LOH on their respective chromosomes. The results of this study will be broadly relevant, both in terms of population-wide genetic architecture of thelytoky, but also for general mechanisms maintaining heterozygosity, i.e. the interplay between recombination and selection via LOH-blocking loci. The mechanisms maintaining heterozygosity are particularly relevant for many fragmented and inbred species of which some suffer from LOH and others not as much.

• DFG Programme: Research Grants