Dmrt1 polymorphism covaries with sex‐determination patterns in Rana temporaria

Abstract

Patterns of sex‐chromosome differentiation and gonadal development have been shown to vary among populations of Rana temporaria along a latitudinal transect in Sweden. Frogs from the northern‐boreal population of Ammarnäs displayed well‐differentiated X and Y haplotypes, early gonadal differentiation, and a perfect match between phenotypic and genotypic sex. In contrast, no differentiated Y haplotypes could be detected in the southern population of Tvedöra, where juveniles furthermore showed delayed gonadal differentiation. Here, we show that Dmrt1, a gene that plays a key role in sex determination and sexual development across all metazoans, displays significant sex differentiation in Tvedöra, with a Y‐specific haplotype distinct from Ammarnäs. The differential segment is not only much shorter in Tvedöra than in Ammarnäs, it is also less differentiated and associates with both delayed gonadal differentiation and imperfect match between phenotypic and genotypic sex. Whereas Tvedöra juveniles with a local Y haplotype tend to ultimately develop as males, those without it may nevertheless become functional XX males, but with strongly female‐biased progeny. Our findings suggest that the variance in patterns of sex determination documented in common frogs might result from a genetic polymorphism within a small genomic region that contains Dmrt1. They also substantiate the view that recurrent convergences of sex determination toward a limited set of chromosome pairs may result from the co‐option of small genomic regions that harbor key genes from the sex‐determination pathway.

A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

“…The X and Y chromosomes are most differentiated in Ammarnäs, where both F ST and sex‐biased heterozygosity are elevated along most of the chromosome, a region of about 125 Mb (Figure , Table and Appendix ). The region is centred on Dmrt1 , which is the putative male‐determining locus in Rana temporaria (Ma, Rodrigues, Sermier, Brelsford, & Perrin, ; Rodrigues et al, ). This pattern is expected: previous coalescent models (Kirkpatrick et al, ) and new models described below show that differentiation between sex chromosomes is expected to be greatest in the SDR.…”

Phylogeography, more than elevation, accounts for sex chromosome differentiation in Swiss populations of the common frog ( Rana temporaria )*

“…Although our dataset cannot disentangle the confounding effect of phylogeny, anecdotal evidence suggests a similar contrast in Swedish populations, where X 1 occurs at high frequency in a Y C population with differentiated sex chromosomes (Ammarnäs), but is rare in a Y B population with proto‐sex chromosomes (Tvedöra; Ma et al. ). Sampling over a larger geographical scale might help test whether X 1 frequency is entirely explained by Dmrt1 Y haplogroups (i.e., phylogeography), or also varies independently with the extent of X‐Y differentiation.…”

“…; Ma et al. ; Table ) with QIAGEN Multiplex Master Mix and 3 µL (mix 1, four Dmrt loci corresponding to length polymorphisms in introns 1, 2, and 5 of Dmrt1 and intron 1 of Dmrt3 ) or 1 µL (mixes 2 and 3, LG2‐A and LG2‐B mixes, corresponding to sex‐linked microsatellites spread over Chr01) of extracted DNA. PCR was performed as follows: after an initial denaturing stage (95°C for 15 minutes), 35 cycles of (94°C for 30 seconds, 55°C (mix 1) or 57°C (mixes 2 and 3) for 1 minute 30 seconds, 72°C for 1 minute), followed by a final extension stage of 60°C for 30 minutes.…”

“…; Ma et al. ). Further south, populations with XX males and non‐GSD have been documented in lowland Switzerland (e.g., Cossonay; 46° 36′ 51″ N, 6° 29′ 22″ E, 562 m asl; Rodrigues et al.…”

“…In between are XY° males with proto‐sex chromosomes, only differentiated from XX individuals at a very small segment comprising Dmrt1 (Ma et al. ; Rodrigues et al. ).…”