Why Chromosome Palindromes?

Abstract

We look at sex-limited chromosome (Y or W) evolution with particular emphasis on the importance of palindromes. Y chromosome palindromes consist of inverted duplicates that allow for local recombination in an otherwise nonrecombining chromosome. Since palindromes enable intrachromosomal gene conversion that can help eliminate deleterious mutations, they are often highlighted as mechanisms to protect against Y degeneration. However, the adaptive significance of recombination resides in its ability to decouple the evolutionary fates of linked mutations, leading to both a decrease in degeneration rate and an increase in adaptation rate. Our paper emphasizes the latter, that palindromes may exist to accelerate adaptation by increasing the potential targets and fixation rates of incoming beneficial mutations. This hypothesis helps reconcile two enigmatic features of the “palindromes as protectors” view: (1) genes that are not located in palindromes have been retained under purifying selection for tens of millions of years, and (2) under models that only consider deleterious mutations, gene conversion benefits duplicate gene maintenance but not initial fixation. We conclude by looking at ways to test the hypothesis that palindromes enhance the rate of adaptive evolution of Y-linked genes and whether this effect can be extended to palindromes on other chromosomes.

Dynamic evolution of great ape Y chromosomes

“…Palindromes are hypothesized to evolve to allow ampliconic genes to withstand high mutation rates on the Y via gene conversion in the absence of interchromosomal recombination (12,13) . Two human palindromes-P6 and P7-do not harbor any genes, however the large proportions of their sequences are present and are multi-copy ( Fig.…”

“…The ampliconic regions consist of repetitive sequences that have >50% identity to each other (7) and contain palindromes -inverted repeats (separated by a spacer) up to several megabases long whose arms are >99.9% identical (12) . Palindromes are thought to evolve to allow intrachromosomal (Y-Y) gene conversion which rescues the otherwise non-recombining male-specific regions on the Y from deleterious mutations (13) . We presently lack knowledge about how conserved palindrome sequences are across great apes.…”

Patterns of Inter-Chromosomal Gene Conversion on the Male-Specific Region of the Human Y Chromosome

“…This situation is similar to that observed by Lange et al (2009) within ampliconic sequences, where both crossover and non-crossover (gene conversion) pathways are active between Y chromosome palindrome arms (Lange et al, 2009; Trombetta and Cruciani, 2017). A model has been proposed in which Y–Y gene conversion may be useful in protecting Y chromosome against its evolutionary degradation (Charlesworth, 2003; Rozen et al, 2003; Connallon and Clark, 2010; Marais et al, 2010; Betrán et al, 2012; Hallast et al, 2013; Trombetta and Cruciani, 2017), by facilitating the efficient removal of Y-linked deleterious alleles from the population. This model can be difficult to apply to X-to-Y gene conversion.…”

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

“…Recent analyses show that a few genes have been conserved due to purifying selection (Hughes et al 2012) and that new genes that are important for male fertility have been transferred to the Y (Lahn et al 2001). Retention of these "essential" male genes is aided by their frequent occurrence in palindromes where intrachromosomal gene conversion decreases the chance of loss and may also foster fixation of new genes by adaptive evolution (Betrán et al 2012).…”

“…In addition to their role in gender determination, sex chromosomes are fascinating because the homologs often differ in gene content and morphology (Vallender and Lahn 2004;Graves 2006;Arunkumar et al 2009;Betrán et al 2012). Their unequal distribution between sexes also means that sexlinked genes experience and respond to evolutionary forces in different ways compared with autosomes (Charlesworth et al 1987;Rice 1987;Charlesworth 1991;Rice 1994).…”