Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta

• Published in: Cells (Basel, Switzerland) Vol. 11; no. 7; p. 1118
• Main Authors: Nanda, Indrajit, Schories, Susanne, Simeonov, Ivan, Adolfi, Mateus Contar, Du, Kang, Steinlein, Claus, Alsheimer, Manfred, Haaf, Thomas, Schartl, Manfred
• Format: Journal Article
• Language: English
• Published: Switzerland MDPI AG 25-03-2022; MDPI
• Subjects: Androgens; Animals; Color; Cyprinodontiformes - genetics; Evolution; Female; Females; Fish; Heterochromatin; Hypotheses; Male; Males; meiosis; MLH1 protein; Pachytene; Poecilia - genetics; recombination; Reptiles & amphibians; Sex chromosomes; Sex Chromosomes - genetics; Sex linkage; Sexual dimorphism; Single-nucleotide polymorphism; synaptonemal complex; Wetlands; Y Chromosome - genetics; Y chromosome degeneration; Y chromosomes; Germany; sexual antagonistic genes; meiosis; recombination; testosterone; 5-methylcytosine; sex chromosomes; Y chromosome degeneration; synaptonemal complex; heterochromatin; sex linked pigmentation pattern
• ISSN: 2073-4409; 2073-4409
• DOI: 10.3390/cells11071118

The conspicuous colour sexual dimorphism of guppies has made them paradigmatic study objects for sex-linked traits and sex chromosome evolution. Both the X- and Y-chromosomes of the common guppy (
) are genetically active and homomorphic, with a large homologous part and a small sex specific region. This feature is considered to emulate the initial stage of sex chromosome evolution. A similar situation has been documented in the related Endler's and Oropuche guppies (
) indicating a common origin of the Y in this group. A recent molecular study in the swamp guppy (
) reported a low SNP density on the Y, indicating Y-chromosome deterioration. We performed a series of cytological studies on
to show that the Y-chromosome is quite small compared to the X and has accumulated a high content of heterochromatin. Furthermore, the Y-chromosome stands out in displaying CpG clusters around the centromeric region. These cytological findings evidently illustrate that the Y-chromosome in
is indeed highly degenerated. Immunostaining for SYCP3 and MLH1 in pachytene meiocytes revealed that a substantial part of the Y remains associated with the X. A specific MLH1 hotspot site was persistently marked at the distal end of the associated XY structure. These results unveil a landmark of a recombining pseudoautosomal region on the otherwise strongly degenerated Y chromosome of
. Hormone treatments of females revealed that, unexpectedly, no sexually antagonistic color gene is Y-linked in
. All these differences to the
group of guppies indicate that the trajectories associated with the evolution of sex chromosomes are not in parallel.