Estimating Tempo and Mode of Y Chromosome Turnover: Explaining Y Chromosome Loss With the Fragile Y Hypothesis

Abstract

Chromosomal sex determination is phylogenetically widespread, having arisen independently in many lineages. Decades of theoretical work provide predictions about sex chromosome differentiation that are well supported by observations in both XY and ZW systems. However, the phylogenetic scope of previous work gives us a limited understanding of the pace of sex chromosome gain and loss and why Y or W chromosomes are more often lost in some lineages than others, creating XO or ZO systems. To gain phylogenetic breadth we therefore assembled a database of 4724 beetle species' karyotypes and found substantial variation in sex chromosome systems. We used the data to estimate rates of Y chromosome gain and loss across a phylogeny of 1126 taxa estimated from seven genes. Contrary to our initial expectations, we find that highly degenerated Y chromosomes of many members of the suborder Polyphaga are rarely lost, and that cases of Y chromosome loss are strongly associated with chiasmatic segregation during male meiosis. We propose the "fragile Y" hypothesis, that recurrent selection to reduce recombination between the X and Y chromosome leads to the evolution of a small pseudoautosomal region (PAR), which, in taxa that require XY chiasmata for proper segregation during meiosis, increases the probability of aneuploid gamete production, with Y chromosome loss. This hypothesis predicts that taxa that evolve achiasmatic segregation during male meiosis will rarely lose the Y chromosome. We discuss data from mammals, which are consistent with our prediction.

Coleoptera Karyotype Database

“…Karyotypes are a highly variable and complex trait that offers an opportunity to detect changes in genome organization, uncover phylogenetic history, and distinguish cryptic species. Our initial analyses show that using the Coleoptera karyotype data to model sex-chromosome evolution can reveal important insights into the evolution of beetle genomes (Blackmon and Demuth 2014). Additionally, in cases where whole genome sequencing is being done, karyotypes offer a quick and inexpensive form of preliminary data providing important guidance in choosing species that will be most informative for answering specific biological questions.…”

How to identify sex chromosomes and their turnover

“…Despite the growing awareness that sex chromosomes have evolved independently many times throughout eukaryotes, our understanding of the processes driving the formation and turnover of new sex chromosome systems is limited and many unanswered questions remain. A large body of theoretical work outlines predictions for when and why sex chromosome transitions occur (Beukeboom & Perrin, ), including genetic drift (Bull & Charnov, ; Saunders, Neuenschwander, & Perrin, ), mutation load on the sex‐limited chromosomes (Blaser, Grossen, Neuenschwander, & Perrin, ; Blaser, Neuenschwander, & Perrin, ), selection on sex ratio (Jaenike, ; Werren & Beukeboom, ) and sexually antagonistic selection (van Doorn & Kirkpatrick, , ), yet attempts to empirically test these have been restricted to a few clades (Blackmon & Demuth, ; Jeffries et al, ; Kitano & Peichel, ; Wright et al, ). Identifying the evolutionary and genomic mechanisms predicted to drive sex chromosome turnover is a major priority, which in turn will shed light on why sex determination is labile in some taxa and not in others.…”

The Genetics of Sex: Exploring Differences

“…Xy+ are sex chromosome bivalents that display distance pairing (no synapsis) and thus do not recombine, allowing the authors to distinguish how differences in sex chromosome pairing and meiotic recombination influence the evolution of the sex chromosomes in two major beetle lineages, Adephaga (which have only XY and XO species), and Polyphaga (where over half of all species are Xy+). Blackmon and Demuth (2014) find that in Adephaga, new Y chromosomes are evolving at the same rate as they are lost, whereas in Polyphaga Y chromosomes are twice as readily gained as lost. The authors propose that different meiotic mechanisms that evolve to ensure sex chromosome segregation affect the tempo of Y chromosome gain and loss.…”

“…Taken further, as essential genes move from the sex chromosome to autosomes, sex chromosomes can be lost and replaced with new ones that evolve from ancestral autosomes. Blackmon and Demuth (2014) used phylogenetic analysis to reveal the tempo of Y chromosome turnover in Coleoptera. They analyzed karyotypes of 4724 beetle species that have heterogametic males that are XY, XO, or Xy+.…”

“…Two studies focus on the biology of reproduction: the transition from predominantly sexual reproduction to asexuality in fungi (Solieri et al 2014) and self-incompatibility in plants (Leducq et al 2014). Two other articles examine differences in the evolution of sex chromosomes: Blackmon and Demuth (2014) look at the evolutionary turnover of sex chromosomes in beetles and Kirkpatrick and Guerrero (2014) use the recombining region of sex chromosomes to measure the strength of sexually antagonistic selection. Finally, two studies focus on gametogenesis-sex differences in meiosis in Caenorhabditis elegans (Checchi et al 2014) and the specification and development of germinal cells in maize (Zhang et al 2014).…”