Interview with the author: A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

In this Blog post, we hear from Dr. Melissa Toups on how new sex chromosomes can evolve! Mellisa and her colleagues show that reciprocal translocations can incorporate large pieces of chromosome into a sex-determining region, thus making the to be co-inherited as sex chromosomes. Join us in learning more about this exciting research directly from Mellisa.

Picture by Christophe Dufresnes

What led to your interest in this topic / what was the motivation for this study? 
I’m interested in the diversity of genetic sex-determination mechanisms. Ranid frogs are a fantastic study species for this because sex determination moves between chromosomes on a fast evolutionary time scale. In Rana temporaria, the study species for this paper, sex chromosome arrangements differ between populations.  We knew from previous linkage maps using microsatellites that the southernmost population had only one small sex-determining region, one northern population had one a larger sex-determining region on the same chromosome, and finally a second northern population had two sex chromosomes formed by reciprocal translocation, which occurs when two chromosomes swap arms and become coinherited.  This was a great opportunity to use genomic techniques to study three different arrangements of sex chromosomes within a single species.

What difficulties did you run into along the way? 
During breeding season, frogs migrate to nearby ponds.  In the evening, the males swim around and sing to females. The successful males attach to females, and we catch them as a couple.  The two northernmost populations, Kilpisjärvi and Ammarnas, breed at the roughly the same time.  We started in Ammarnas, but catching the frogs we needed took longer than expected.  By the time we arrived in Kilpisjärvi, breeding season was almost over.  Most of the frogs remaining in the ponds were single males. We were only able to catch two breeding pairs, and we were lucky enough to eventually find two solo females, but it took weeks of effort, which was nerve-wracking. \

What is the biggest or most surprising finding from this study? 
We are the first to use genomic techniques to characterize a reciprocal translocation of a sex chromosome. We don’t know how common these rearrangements are because they are only cytologically detectable at pairing during meiosis.  Here, we show that they can incorporate large regions of an additional chromosome into the sex-determining region, which are subject to very different selective forces than the autosomes.  The most surprising finding was detecting evidence for another small nonrecombining region in Kilpisjärvi on a different chromosome. These frogs are full of surprises!

Moving forward, what are the next steps for this research?
We are currently investigating whether different sex chromosome arrangements affect male gene expression.  To answer this question, we are focusing on an alpine population of Rana temporaria in Switzerland that has males with two types of Y chromosomes.  Some Y chromosomes only differ from the X chromosome in a small region around the sex-determining locus, and other Y chromosomes are differentiated from the X chromosome throughout their length. We are also working on using high-density linkage mapping of RAD sequences to confirm the novel sex-chromosome rearrangement in the Kilpisjärvi populations.

What would your message be for students about to start their first research projects in this topic? 
Our standard models for sex-chromosome evolution are mostly based on the mammalian XY system, which are more than 160 million years old.  However, the more organisms we study, the more we realize that ancient, highly diverged sex chromosomes may be the exception rather than the rule. My message would be to keep an open mind about what you might find, and let your organism surprise you!

What have you learned about science over the course of this project? 
One thing I’ve learned working on this project is the importance of assembling a team of researchers with complementary strengths.  Each person brought unique and critical skills to this project. We were able to combine knowledge of our study system, bioinformatics, and coalescent modeling to produce a comprehensive examination at sex chromosomes in Rana temporaria.

Describe the significance of this research for the general scientific community in one sentence.
We provide the first genomic view of an entirely different way that new sex chromosomes can evolve.

Describe the significance of this research for your scientific community in one sentence.
We show that the reciprocal translocations can dramatically increase the portion of the genome that is incorporated into the sex-determining region.

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