Fish Species’ Y Chromosomes Diverged Even Without Recombination

ABOVE: Five morphs of Poecilia parae—from top: melanzona yellow, melanzona blue, melanzona red, parae, immaculata—and a female (bottom) of the same species
CLARA LACEY

EDITOR’S CHOICE IN EVOLUTION

The paper
B.A. Sandkam et al., “Extreme Y chromosome polymorphism corresponds to five male reproductive morphs of a freshwater fish,” Nat Eco Evol, 5:939–48, 2021.

One of the key stages in the evolution of different sex chromosomes is a loss of recombination—the exchange of DNA during meiosis—that is both an important mechanism for maintaining genetic diversity in populations and for purging damaging mutations. This loss has led to the gradual depletion of functional gene content from the Y chromosome in many species, says Judith Mank, an evolutionary geneticist at the University of British Columbia who studies sexual dimorphism.

Nevertheless, some species have high levels of male phenotypic variability that appear to be Y-linked. The freshwater fish and guppy relative Poecilia parae, for example, has five different male morphs that vary in size, coloration, and behavior. So-called parae males are large, silvery, and aggressive to other fish, for example, while blue melanzona males are smaller, sport stripes, and rely on their looks to attract females. 

These morphs coexist alongside one another, Mank says, and their traits are reliably passed from fathers to male offspring, indicating the variation is sex-linked. Interested in whether the genetic source of this variation could be hiding in P. parae’s Y, Mank and her colleagues used linked-read DNA sequencing on tail samples from 40 fish collected in Guyana, and the results confirmed the researchers’ hunch: “There were really big differences in [Y chromosome] size and gene content” between the morphs, Mank says. The morphs’ Ys were more similar to one another than they were to the Y chromosome of a sister fish species, supporting the idea that the variation arose after, not before, speciation. 

That such variation arose despite low levels of genetic recombination on this chromosome suggests that other diversity-generating mechanisms, such as the movement of transposable elements, may be at play, Mank adds. 

University of Edinburgh evolutionary biologist Deborah Charlesworth, who studies guppies and was not involved in the work, says she was pleased to see research on wild P. parae populations that seems to confirm the Y chromosome’s role in controlling coloration and other traits. It would be interesting to learn more about the function of these sequences—are they protein-coding, or do they perhaps have a regulatory role?—and about their location on the chromosome, she adds. “What are these genes and where are they?”