What are the genomic causes and consequences of the evolutionary transitions in sex determination?

Sex Chromosome Evolution

TSD appears to be the ancestral state in turtles, and GSD has evolved multiple times in different lineages (Valenzuela and Adams 2011, Sabath et al. 2016), yet little is known about the sex chromosome systems that evolved during the repeated transitions from TSD to GSD. Through a collaborative NSF-funded project (MCB 0815354 - S.V. Edwards CoPI, Harvard University), we tackle the evolution of sex chromosomes and of sex-linked genes, identifying additional sex chromosome systems in turtles and investigating the molecular evolution of the genes they contain.

During an early collaboration, we used comparative genome hybridization and discovered the existence of a cryptic XY sex chromosome system in a GSD turtle from Australia (Chelodina longicollis), which involved a pair of micro-chromosomes (Ezaz et al. 2006). This was the first such report for turtles. A follow up study in a closely related species (Emydura macquarii) revealed a similar cryptic XY system of macro-chromosomes (Martinez et al. 2008). More recent data on Apalone spinifera uncovered a ZW system in this species, and revealed an intriguing conservation in the sex chromosomes of Trionichid turtles compared to the morphological divergence seen in Chelid turtles (Badenhorst et al. 2013). Our work also permitted the identification of the youngest turtle sex chromosome system in Glyptemys insculpta (XX-XY) (Montiel et al. 2016).

Our more recent research avenues involved the study of dosage compensation in turtles and the epigenetics of sex determination.

Co-evolution of chromosome number and sex determination

We detected an startling association in turtles, where chromosome number evolves 20 times faster in phylogenetic branches of the turtle tree of life where there is an evolutionary transition in sex determining mechanism (from TSD to GSD or viceversa), and this transitions coincide with peaks or lows in global temperature over more than 200 years of turtle evolution, linking climate change as a potential ecological force fueling this process (Valenzuela and Adams 2011).

Thanks to another NSF grant (MCB 1244355), we combine molecular cytogenetics and transcriptomics approaches to better understand the functional nature of this association and the ultimate forces responsible for shaping this pattern. We are using multidirectional chromosome painting to reconstruct the ancestral turtle karyotype and to identify chromosomal breakpoints that accrued during genome evolution across turtle lineages, and the newly sequenced turtle genomes and transcriptomic resources we have developed to identify the link of genome rearrangements and sex determination.

Evolution of Dosage Compensation using turtles as a model system

When sex chromosomes (e.g. XX/XY or ZZ/ZW) evolve in diploid species, genes are lost from the Y or W (or lose their function) as they degenerate over time due to their lower recombination. The inequality of gene copy number causes an imbalance in transcription which may produce sub-optimal or lethal phenotypes, unless a mechanism existed to re-establish a balance. Dosage compensation (DC) is a system to equalize the activity of X- or Z-linked genes to counterbalance the deleterious effects of differential gene copy number. The diversity of dosage compensation remains obscure as well as its causes and consequences. A new NSF grant (IOS 1555999), will help fund a study on the evolution of turtle dosage compensation. Turtles are ideal to study dosage compensation because XX/XY and ZZ/ZW sex chromosomes have evolved independently multiple times, and there are increasing turtle genomic resources.