Mechanisms for overcoming challenges in polyploid evolution in the jewel wasp Nasonia vitripennis

Polyploidy is the heritable condition of having more than the normal number of chromosome sets. It has long been assumed to be an evolutionary dead end, as it causes severe abnormalities including sterility, chemical imbalance of cells, and unbalanced gene expression (dosage compensation). However, polyploidy is now recognized as a major evolutionary force across Eukaryota, driving for example mass speciation, stress adaptation, and gene diversity (through provision of additional gene copies that acquire new functions). Correspondingly, there has been an international call by researchers across biological systems to produce a synthesized understanding of polyploidization’s broad role in evolution by 2030. Particularly, there is a dire need to understand mechanisms by which initial polyploid challenges are overcome in order for downstream benefit to emerge, and to explain why some polyploid lineages are evolutionarily successful and others go extinct. With this proposal we aim to use the genetic model species Nasonia to better understand the immediate challenges of polyploidization. Polyploidy is notoriously difficult to study in animals due to few means to experimentally induce it, and polyploidized individuals are usually sterile. Yet, polyploids of the jewel wasp Nasonia are reproductively capable, and there are multiple means to induce Nasonia polyploidy. Like all hymenopterans (the large and diverse order of ants, bees, sawflies, and wasps), N. vitripennis has haplodiploid sex determination. Unfertilized eggs develop into haploid males and fertilized eggs develop into diploid females. Polyploids (diploid males, triploid females) can be studied in the long-maintained Whiting Polyploid Line (WPL) or newly generated by parental RNAi knockdown (KD) of several sex determination genes (transformer, transformer-2, and womanizer). We recently reported that WPL polyploids have high male fitness but low female fecundity. In contrast, in surprising divergence from not just the WPL but all studied polyploid hymenopterans, a newly generated tra KD line had inferior diploid males but highly fertile triploid females with reduced aneuploidy. Also, the WPL exhibited cell number reduction, a polyploid adaptation to prevent gigantism (previously only known from vertebrates), but the tra KD line did not. Preliminary analysis of two housekeeping genes indicated no gene dosage differences; a sex-linked dosage compensation pattern seems conserved regardless of ploidy or genetic background. These studies provide the first empirical evidence of variation in polyploid phenotypes depending on the mode of polyploidization, an oft suggested but hitherto experimentally unsubstantiated hypothesis on why some polyploid lineages thrive and others die out. In this proposal we aim to answer the following questions: (1) how does polyploid phenotype vary between the WPL and newly created lines with differing genetic backgrounds, (2) do polyploids have cell number and/or size reduction mechanisms, (3) how is gene expression and dosage altered following polyploidization, and (4) does chromosome segregation (fecundity) vary depending on polyploidization pathway and lineage age? To meet these objectives we apply for a four-year PhD position at Wageningen University (WU) supervised by Eveline C. Verhulst and a three-year Postdoc position at the University of Groningen (UG) supervised by Leo W. Beukeboom. Results will contribute to our understanding on how polyploidy has and continues to operate as a major force in animal evolution.dge of the evolution of polyploidy among animals, which still has many gaps.