Sex Chromosome Evolution in Willows (Salix spp.)

Date

2023-05

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Abstract

The evolution of sex chromosomes is a fascinating subject in evolutionary biology, particularly in the angiosperm family Salicaceae. Although all species in this family are dioecious, meaning they have separate male and female individuals, they display a remarkable diversity of sex chromosomes, with the sex-determining region located on different chromosomes. In my dissertation, I employed various techniques, including ecology, population genetics, genomics, and phylogenetics, to study the evolution of sex chromosomes in willows (Salix spp.), a genus within Salicaceae. The second chapter of my dissertation aimed to investigate the sexual dimorphism of Salix exigua and Salix nigra. Sexually dimorphic traits have not commonly been documented in willows, but their presence is important because they may influence the movement of sex chromosomes. I measured early spring bud density, catkin number, and flower number per catkin in S. exigua, as well as flower number and catkin number per flower in S. nigra, across four sampling periods. The results indicated that there was no sexual dimorphism in pre-season buds per branch in S. exigua, but males produced more flowers per catkin and more catkins per branch than females in both S. exigua and S. nigra. The presence of reproductive sexual dimorphisms in Salix species provides evidence that sexual selection has the potential to play a role in the evolution of their mating strategies and sex determination system. The third chapter of my dissertation aimed to identify the ancestor of the sex chromosome in the Salix clade. The phylogenetic tree of Salix is ambiguous as to whether the ancestral sex chromosome is chromosome 7 (Chr7) or chromosome 15 (Chr15). Identifying the ancestral state of the sex chromosome is crucial for understanding the evolutionary events during sex chromosome and sex determination evolution. I conducted a comparative genomic analysis and found that patterns of homology on Chr7 and Chr15 across Populus mexicana (the outgroup), S. nigra, and S. exigua indicated that the sex determination locus likely originated on Chr7. Using these results, I was able to reconstruct changes in the gene content and genes controlling sex determination that occurred during the early evolution of willows. In the fourth chapter, I conducted a detailed study in Salix examining the shift from an XY to a ZW sex determination system that occurred in the same location (homologous transition) on chromosome 15 during Salix evolution. First, I discovered that the sex-determination system for S. exigua is on Chr15 and it has XY heterogamety. Based on the phylogeny of Salix and other known sex chromosomes in the genus, I determined that there was an ancient shift from an XY to a ZW sex determination system on chromosome 15. I conducted a detailed comparison of the S. exigua X and Y chromosomes with the S. purpurea Z and W chromosomes to reconstruct the events that resulted in the shift. By utilizing chromosome-level assemblies, half-sib families, and population samples from the wild, I traced the loss of the X chromosome and the transformation of the Y into both the Z and W during this transition. The results suggest that the origins of sex chromosomes during homologous transitions may be more flexible than previously considered. Specifically, both the W and Z chromosomes have arisen from the Y chromosome in willows, which is unexpected since the W chromosome is more likely to arise from the X chromosome due to the feminizing genes they both carry. These findings indicate that the mechanism of sex determination and the unexpectedly low genetic load on the Y chromosome have contributed to the flexibility in the origins of sex chromosomes during homologous transitions. These findings shed new light on the dynamics of sex chromosome evolution in plants and have implications for the understanding of the evolutionary biology of sex determination systems.


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Keywords

Salicaceae, sex determination, XY chromosomes, ZW chromosomes, sexual dimorphism

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