as it involves the rare stabilization of a
handful of inversions and is highly variable
(fig.S4).However,itworksfasterinlarger
populations, as selective interference opposes
recombination arrest and the stabilization of
large strata.
Our model also reverses the causality pro-
posed by previous theories by showing that
dosage compensation can cause recombina-
tion suppression, rather than being a conse-
quence of degeneration after such suppression.
Sexually antagonistic effects are involved in
the evolution of suppressed recombination.
However, they result from the fact that one
sex is heterogametic, not from males and fe-
males having divergent sex-specific optima
for reproductive traits or expression levels.
All genes for which dosage affects fitness
can contribute to the process, not just a sub-
set of sexually antagonistic loci. The poten-
tial sexually antagonistic effect of dosage
compensation has long been appreciated
( 7 , 12 , 28 – 30 ). However, its potential role in
recombination arrest has not been previously
recognized, as it is usually thought to occur
late in the degeneration process. Once re-
combination has stopped, sexually antagonis-
tic alleles can arise and be maintained ( 9 , 31 ),
but they are not required for recombination
arrest, as shown here.
We showed that the emergence of non-
recombining and degenerated sex chromo-
somes in diploid organisms requires very few
ingredients: genetic sex determination, dele-
terious mutations, inversions, sex-specific trans
regulators, and stabilizing selection on gene
expression levels. This theory includes all steps
(Fig. 4 and fig. S8) in a single set of assump-
tions and is compatible with current data on
sex chromosome evolution in chiasmate spe-
cies ( 25 ). It predicts the occurrence of strata,
including small ones ( 16 ) and the occurrence
of early regulatory changes in young sex chro-
mosomes ( 20 – 24 ). It also accounts for the
lack of decisive evidence for a causal role of
sexually antagonistic loci on recombination
arrest ( 16 – 19 ). Overall, this theory explains the
rapid expansion, degeneration, and dosage
compensation of the nonrecombining region
of sex chromosomes without requiring pre-
existing selection pressures favoring sexual
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ACKNOWLEDGMENTS
We thank D. Charlesworth, G. Marais, Y. Michalakis, and four
anonymous reviewers for comments and suggestions and
K.McKeanforediting.WethanktheMBBclusterfromLabex
CEMEB, and the CNRS ABiMs cluster.Funding:This work was
supported by grant GenAsex ANR-17-CE02-0016-01.Author
contributions:Original idea: T.L. and D.R.; Model conception:
T.L. and D.R.; Code: D.R. and T.L.; Simulations: T.L.; Data
analyses: T.L.; Interpretation: T.L. and D.R.; First draft, editing
and revisions: T.L. and D.R.; Project management and funding:
T.L.Competing interests:The authors declare no conflicts
of interest.Data and materials availability:Simulation code is
available at Zenodo ( 32 ).SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abj1813
Materials and Methods
Supplementary Text
Figs. S1 to S8
References ( 33 Ð 46 )
MDAR Reproducibility Checklist26 April 2021; accepted 14 December 2021
10.1126/science.abj1813666 11 FEBRUARY 2022•VOL 375 ISSUE 6581 science.orgSCIENCE
Fig. 4. Steps involved in the evolu-
tion of a Y nonrecombining stratum.
The process involves four steps, as
explained in the text, and is briefly
described by captions on the figure.
Only the first stratum is illustrated,
but steps one to four are repeated for
strata extending the nonrecombining
portion of the until the whole
chromosome is degenerated, silenced,
and dosage-compensated.
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