Repeat element proliferation on the caenophidian W chromosome

Alderman, Megan G.

hbs5rf@virginia.edu

Farleigh, Keaka                                                                                                                                             

Highland, Dylan K.                                                                                                                                          

Schield, Drew

Department of Biology                                                                                                                              

University of Virginia                                                                                                                            

Charlottesville, Virginia USA

Caenophidan snakes exhibit ZW sex determination, with heterogametic ZW sex chromosomes in females and homogametic ZZ males. As sex chromosomes evolve, selection may favor linkage between a sex-determining locus and sexually antagonistic alleles, leading to recombination suppression between the Z and W chromosomes. Because these W-linked regions no longer experience sexual recombination, they are susceptible to mutation accumulation, including increased rates of genomic repeat proliferation due to transposable element (TE) activity, as seen in studies of XY systems (e.g., Drosophila) and other ZW systems (e.g., birds). Such repeat proliferation may constitute sex-biased mutational load, with impacts on genome regulation, female fitness, and hybrid incompatibility. A previous study demonstrated that the prairie rattlesnake (Crotalus viridis) W chromosome is over 80% repetitive and houses a disproportionately large quantity of TEs, yet these broader perspectives on TE proliferation in snakes are still needed. We address this gap in knowledge by studying female genomes sampled from across the broader Caenophidian clade, including high-quality genomes for representative species in the Viperidae, Colubridae, and Elapidae). We identified and annotated W-linked genomic regions, finding that W chromosomes are highly repeat-rich across all taxa and house a disproportionately high proportion of TEs relative to the rest of the genome, constituting genomic refugia for full-length TEs potentially capable of self-replication. We also find dynamic evolution of distinct TE families on Caenophidian W chromosomes, with distinct major expansions characteristic of the highly-heteromorphic viperid W chromosome. Finally, we assessed the “toxicity” of the W by quantifying the proportion of full-length LTR retrotransposons in the heterogametic sex relative to the homogametic sex, finding that the W chromosome contributes excess female-biased mutational load in Caenophidian snakes. Our findings suggest that, while W-linked genes play important putative roles in female fitness, the W chromosome nonetheless acts as a source of intragenomic conflict and may constitute a hotspot for postzygotic reproductive isolation between species.